Prenatal tobacco prevention and cessation interventions for women in low- and middle-income countries

Article (PDF Available)inActa Obstetricia Et Gynecologica Scandinavica 89(4):442-53 · March 2010with32 Reads
DOI: 10.3109/00016341003678450 · Source: PubMed
Although the prevalence of tobacco use is decreasing in many high-income countries, it is increasing in many low- and middle-income countries. The health and economic burden of increasing tobacco use and dependence is predictable and will have devastating effects in countries with limited resources, particularly for vulnerable populations such as pregnant women. We sought to review effective tobacco prevention and intervention strategies for decreasing tobacco use and secondhand smoke exposure before and during pregnancy in high-, middle-, and low-income countries. We reviewed several types of interventions, including population-level efforts (increasing tobacco prices, implementing tobacco control policies), community interventions, clinical interventions, and pharmacological treatments. A second purpose of this report is to present findings of an international expert working group that was convened to review the evidence and to establish research priorities in the following areas: (a) preventing the uptake and reducing tobacco use among girls and women of reproductive age; and (b) reducing tobacco use and secondhand smoke exposure among pregnant women. The working group considered the evidence on existing interventions in terms of burden of disease, intervention impact, intervention costs, feasibility of integration into existing services, uniqueness of the contribution, and overall feasibility. Finally, we present the working group's recommendations for intervention research priorities.
Acta Obstetricia et Gynecologica. 2010; 89: 442453
Prenatal tobacco prevention and cessation interventions for women in
low- and middle-income countries
Department of Medicine and Department of Obstetrics and Gynecology, University of Connecticut School of Medicine,
Farmington, Connecticut, USA,
Division of Reproductive Health, Centers for Disease Control and Prevention, Atlanta,
Georgia, USA,
Department of Mother & Child Health Research, Institute for Clinical Effectiveness and Health Policy,
Buenos Aires, Argentina,
Department of Obstetrics and Gynecology, Oregon Health and Science University, Portland,
Oregon, USA,
Global Network for Perinatal and Reproductive Health, Portland, Oregon, USA,
Department of
Obstetrics and Gynecology , Thomas Jefferson University, Philadelphia, Pennsylvania, USA,
Department of Obstetrics
and Gynecology, Drexel University School of Medicine, Philadelphia, Pennsylvania, USA,
Division of Epidemiology and
Community Health, School of Public Health, University of Minnesota, Minneapolis, Minnesota, USA,
Keck School of
Medicine, University of Southern California, Los Angeles, California, USA, and
National Cancer Institute, Tobacco
Control Research Branch, Bethesda, Maryland, USA
Although the prevalence of tobacco use is decreasing in many high-income countries, it is increasing in many low- and middle-
income countries. The health and economic burden of increasing tobacco use and dependence is predictable and will have
devastating effects in countries with limited resources, particularly for vulnerable populations such as pregnant women. We
sought to review effective tobacco prevention and intervention strategies for decreasing tobacco use and secondhand smoke
exposure before and during pregnancy in high-, middle-, and low-income countries. We reviewed several types of interven-
tions, including population-level efforts (increasing tobacco prices, implementing tobacco control policies), community
interventions, clinical interventions, and pharmacological treatments.
A second purpose of this report is to present ndings of an international expert working group that was convened to review the
evidence and to establish research priorities in the following areas: (a) preventing the uptake and reducing tobacco use among
girls and women of reproductive age; and (b) reducing tobacco use and secondhand smoke exposure among pregnant women.
The working group considered the evidence on existing interventions in terms of burden of disease, intervention impact,
intervention costs, feasibility of integration into existing services, uniqueness of the contribution, and overall feasibility. Finally,
we present the working groups recommendations for intervention research priorities.
Key words: Global, tobacco, perinatal and reproductive health
Currently, an estimated 5.4 million people worldwide
die each year from tobacco use (1). In the course of
the next 30 years, tobacco-related deaths are expected
to increase to 8 million each year; 80% of these deaths
are projected to occur in low- and middle-income
countries (LMICs). While far more men than women
Correspondence: Cheryl A. Oncken, Department of Medicine and Department of Obstetrics and Gynecology, MC 3940, University of Connecticut School of
Medicine, 263 Farmington Avenue, Farmington, CT 06030-3940, USA. E-mail:
The ndings and conclusions are those of the authors and do not necessarily represent the ofcial position of the Centers for Disease Control and Prevention
or the National Cancer Institute.
(Received 10 November 2009; accepted 3 February 2010)
ISSN 0001-6349 print/ISSN 1600-0412 online 2010 Informa UK Ltd. (Informa Healthcare, Taylor & Francis AS)
DOI: 10.3109/00016341003678450
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use tobacco in LMICs, surveillance data from the
Global Youth Tobacco Surveys suggest that the dif-
ference between the two sexes is narrowing (2).
Women and their offspring face additional health
risks if women smoke cigarettes during pregnancy,
as smoking by pregnant women increases the risk of
low birthweight, prematurity, placenta previa,
placental abruption, preterm premature rupture of
membranes, and sudden infant death syndrome
(SIDS) (3). The risks of maternal smokeless tobacco
use (e.g. snuff or chewing tobacco) are less studied, but
the available evidence shows an increased risk of still-
birth, low birthweight, prematurity, and infant death
(4,5). Waterpipe smoking may increase the risk of
delivering a low birthweight infant as well as other
pregnancy complications (6,7). Secondhand smoke
(SHS) exposure to infants causes increased risk of
SIDS and lower respiratory illness (8). Current efforts
to address the overall globalization of tobacco focus on
tobacco use among all populations. In 2003 the
World Health Assembly adopted the World Health
Organization (WHO) Framework Convention on
Tobacco Control (FCTC) in response to the globali-
zation of the tobacco epidemic (9). The FCTCsgoalis
to protect the health of citizens and many of its 38
articles address health-related topics such as safeguard-
ing of public health policies with respect to tobacco
control from commercial and other vested interests of
the tobacco industry; protection from exposure to
tobacco smoke; packaging and labeling of tobacco
products; and tobacco advertising, promotion, and
sponsorship. The WHO published its rst Report
on the Global Tobacco Epidemic, in 2008, which
presented the MPOWER framework for tobacco
control (1). This framework calls for monitoring of
the tobacco epidemic; offering assistance to quit; pro-
tecting nonsmokers from exposure to SHS; warning
smokers of the health effects of smoking; enforcing
advertising bans; and raising taxes on tobacco pro-
ducts. While the MPOWER framework does not
directly address pregnant women, many of its strategies
will reduce prenatal tobacco exposure. Pregnant
women, nonetheless, are a special population with
some unique needs regarding tobacco control.
Although tobacco use is decreasing in most high-
income countries, it is on the rise in many LMICs
among girls and women of reproductive age.
The prevalence of cigarette smoking among girls
aged 1315 ranged from 2% in Southeast Asia and
the Eastern Mediterranean region to 17% in Europe
(Figure 1) (2). The prevale nce of other tobacco use
[e.g. p ipes, waterpipes, smokeless tobacco, and bidis
(thin, hand-rolled cigarettes)] among girls was
generally higher tha n that of cigarette use in several
regions and ranged from 6% in the Western Pacic
region to 11% in Africa (2). A potential high
concordance of tobacco use in pregnant and non-
pregnant women in LMICs highlights the need for
prevention and cessation in terventions to target both
pregnant and reproductive age women.
Prevention and cessation programs for pregnant
women have been studied extensively in high-incom e
Africa Americas Europe Southeast
West Pacific
Other tobacco
Figure 1. Self-reported tobacco use among girls aged 1315 years by WHO region: Global Youth Tobacco Survey, 20002007.
Decreasing tobacco exposure dur ing pregnancy 443
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countries; however, few studies testing interventions
have been conducted in LMICs. We sought to pro-
vide a comprehensive review of interventions to
decrease tobacco exposure before and during preg-
nancy in high-, middle-, and low-income countries
and to discuss relevant considerations for adopting
and evaluating interventions in LMICs. We also
present ndings of an internationa l expert working
group that was convened to review the evidence and
to establish research priorities.
Material and methods
We conducted a search of peer-reviewed articles on
interventions (ranging from clinical to population-
level) in the databases of Pubmed, the Cochrane
Library, Global Health, and the WHO regio nal libra-
ries of Latin America, Africa, the Eastern Mediterra-
nean region, and South East Asia. We searched for
articles from January 1975 to June 2009 using several
keywords and keyword combinations (e.g. pregnancy,
smoking cessation, tobacco, smokeless tobacco, envi-
ronmental tobacco smoke, tobacco smoke pollution,
waterpipe). We reviewed articles with English- or
Spanish-languag e abstracts. When possible, we
limited our searches to randomized-controlled trials.
We used existing meta-analyses or consensus
opinions assessing interven tions for tobacco preven-
tion, cessation, or reduced tobacco exposure. We
also queried via email tobacco control professionals
who are members of the Society for Research on
Nicotine and Tobacco and GL OBALink to nd
additional completed or ongoing studies of interven-
tions tested in LMICs. Countries were categorized as
low-, middle-, or high-income using the World
Banks July 2009 economy classication, which is
based on the gross national income per capita (10).
Our search yielded 417 articles. We excluded articles
that did not assess clinical or population-level inter-
ventions. Of the 44 articles that met our inclusion
criteria, 18 were meta-analyses or systematic reviews,
and 26 were individual studies; 11 studies were con-
ducted in LMICs (1121).
Time periods for interventions to reduce tobacco exposure
A range of clinical and population-level interventions
have been used to decrease maternal tobacco
exposure, including interventions that can be insti-
tuted in adolescence to prevent to bacco initiation,
before pregnancy or during pregn ancy to increase
cessation. Table 1 shows interventions targeting
each of these time windows that have been shown
to be effective based on systematic reviews, some of
which include meta-analyses. The majority of reviews
focused on interventions targeting cigarette smoking
(2228), with some targeting smokeless tobacco use
(chewing tobacco or snuff) (22,29). We found no
Table 1. Effective interventions to decrease initiation and increase cessation of tobacco use, by time period.
(at any time)
Cessation before
during pregnancy
Increasing unit price for tobacco products X
Advertising bans in most or all available media X
Mass media combined with other interventions
(e.g. in schools)
Reducing client expense for cessation therapies X
Systems interventions (screening systems,
provider training, coverage of treatment)
Clinical interventions (e.g. physician or nurse
advice, or counseling)
Pharmacotherapy X
Relapse prevention
Hopkins et al. (24).
National Cancer Institute (23).
Fiore et al. (22).
Lumley et al. (27).
Hughes et al. (26) and Stead et al. (28).
Pharmacotherapy has been shown to be effective for reducing cigarette use [Fiore et al. (22)], but not smokeless tobacco use in
non-pregnant users [Ebbert et al. (29)].
Hajek et al. (25).
444 C.A. Oncken et al.
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interventions on other forms of smoked or smokeless
tobacco, and a Cochrane review found no interven-
tions targeting waterpipe use (30).
Population-level interventions/tobacco control
Interventions to prevent initiation or increase cessa-
tion of tobacco use among women of reproductive age
can be implemented at the population (national or
smaller geo-political areas) or individual levels. This
section provides a summary of effective interventions
that are implemented outside of the clinical setting.
Increasing tobacco price. Article 6 of the WHO FCTC
requires countries to implement tax policies, and
where appropriate, price policies ... aimed at reduc-
ing tobacco consumption (9). Interventions that
increase the price of tobacco products reduce tobacco
consumption in both high-income countries and
LMICs (24,31,32). In high-income countries, where
the majority of studies have been conducted, a 10%
increase in cigarette prices would result in a 2.55%
reduction in demand for cigarettes (32). A review
examining price increases in LMICs indicates that
a sustained 10% increase in cigarette prices would
reduce cigarette consumption from 4 to 14% (31),
suggesting that price increases have a greater impact
in LMICs than in high-income countries.
Several studies have evaluated the impact of increas-
ing cigarette prices on use by pregnant smokers. One
study found that a price increase of USD $0.55 per
pack would reduce maternal smoking by 3% points, a
22% reduction in prevalence (33), and another found
that a 10% increase in cigarette taxes would increase
the probability of a woman quitting by 10% (34).
Additionally, a study examining the impact of
increased cigarette prices (from the US Master Settle-
ment Agreement) found that prenatal smoking did
decline, but after adjustment for secular trends, by
less than half than what was predicted by previous
studies (35). Although most studies show that
increases in tobacco taxes decrease smoking rates in
pregnancy, we did not nd either a meta-analysis or a
consensus opinion from an expert panel conrming
effectiveness of this intervention during pregnancy. In
one US study, higher cigarette prices through taxation
and smoking bans and tobacco use restrictions in work
places, child care centers, and restaurants were asso-
ciated with a reduction in deaths due to SIDS; a 10%
increase in cigarette taxes was estimated to reduce
deaths due to SIDS by a range of 1.61.8% (36).
Though reduced tobacco expenditures may release
household income for other es sential expenditures
(e.g. food, healthcare), it is unclear what effect taxa-
tion has on households with continued smokers,
specically low-income households. In the United
Kingdom, spending on tobacco is proportionally
higher among low-income women than among
high-income women, and qualitative data show that
these mothers considered tobacco an essenti al expen-
diture compared with food (37). However, a Chinese
study showed that the relative nancial burden from
additional taxation on cigarettes is lower among low-
income households than among high-income ones
(38). Studies in Indonesia and Bangladesh have
shown that having a smoker in the household diverts
household income from food to tobacco, putting
infants and children at greater risk of chronic malnu-
trition and death (3941). Much work is currently in
progress examining the impact of tobacco prices in
LMICs; however, further research is needed to better
understand positive and negative impacts, especially
among households with pregnant women and infants.
This research needs to carefully consider country-
specic differences in tobacco products, prices, and
approaches to taxation.
Advertising bans. A review of studies examining
tobacco-advertisi ng bans in different countries con-
cluded that comprehensive bans reduce tobacco con-
sumption (23). Partial bans, such as those limiting
content or media venues, were not effective as these
allowed advertising to be shifted to another media.
Countries that restrict all advertising of tobacco pro-
ducts will effectively reduce tobacco consumption.
The WHO FCTC calls for restriction on all adver-
tising, promotions, and sponsorships (9).
Mass media campaigns combined with other interventions.
A recent US National Cancer Institute monograph
concluded that mass media campaigns (through tele-
vision, radio, print, and billboards) designed to dis-
courage tobacco use can change youth attitudes about
tobacco use , curb smoking initiation, and encourage
adult smoking cessation, and that the effect is greater
when campaigns are combined with school- and/or
community-based programming (23). Similarly,
another review found that mass media campaigns
reduce initiation among youth and, when combined
with other interventions (e.g. tobacco tax increases),
increase cessation and reduce tobacco consumption
at the population level (24).
Mass media interventions have also been effective
in decreasing tobacco use in LMICs. Media com-
bined with household interviews, clinical oral exams,
and personal cessation advice have been effective in
reducing tobacco use (smokeless tobacco and
Decreasing tobacco exposure dur ing pregnancy 445
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cigarette smokin g) in large cohort studies conducted
in several communities in India (13,17,18).
Warning labels. Today, most countries require tobacco
product manufacturers to place warning labels on
tobacco packages, because they are an effective way
to warn smokers about the health hazards of tobacco
use, and serve as a rst step toward quitting (42).
However, the impact of warning labels depends upon
many factors, including their size, comprehensive-
ness, visibility, and whether they are printed in the
local language (1). Large graphic (pictorial) warning
labels, which are especially effective, were rst intro-
duced by Cana da in 2000, and have now been imple-
mented in more than 20 countries (43,44). The fact
that the cost of the warning labels are borne by
tobacco manufacturers makes them especially attrac-
tive to LMICs.
Recognizing their importance, Article 11 of the
WHO FCTC requires parties to the treaty to imple-
ment health warnings describing the harmful effects
of tobacco use ; detailed guidelines for governments
to implement effective warning labels were adopted by
the third session of the conference of the parties (9).
Additionally, WHO has called on governments to
require that all tobacco packages include pictorial
warnings (45).
Clinical interventions
In high-income countries, clinical interventions have
been found to be effective in helping both non-
pregnant and pregnant smokers quit. In one meta-
analysis, physician advice to quit increased long-term
cigarette abstinence rates to 10.2% (95% CI 8.5
12.0) compared to no-advice abstinence rates of
7.9% among non-pregnan t women (22). Although
this increase in abstinence rates might seem low,
physician advice to quit is a low-intensity and low-
cost intervention that could have considerable popu-
lation-level impact. Clinics that incorporate a systems
approach to tobacco treatment (i.e. clinician training
and reminder systems) signicantly increase the rate
at which clinicians intervene with their patients who
smoke (22). The 5As model (ask, advise, assess,
assist, arrange follow-up) has been shown to be effec-
tive in increasing quit rates when implemented in
primary care settings in the US. (46). The 2As
and an R model (i.e. ask, advise, and refer) has
also been recommended as a practical tobacco treat-
ment strategy for busy clinics (47). Clinical/behavioral
interventions that are effective in clinical trials include
practical problem solving (general skills training) and
providing smokers with support during treatment.
Practical counseling (104 studies) was associated
with abstinence rates of 16.2% (95% CI 14. 0
18.5), and intra-treatment social support (50 studies)
had abstinence rates of 14.4% (95% CI 12.316.5),
compared to a rate of 11.2% for no counseling (22).
Two meta-analyses have shown that behavioral
strategies increase quit rates in pregnant smokers by
an add itional 6% over those in control groups (22,27).
A Cochrane review included randomized and quasi-
randomized trials (72 studies; approximately 25,000
pregnant smokers) (27). The relative risk for continu-
ing to smoke with a behavioral intervention versus
control was 0.94 (95% CI 0.930.96). Although
smoking cessation interventions appear to have a
modest effect on quit rates, the impact on infant
outcomes is signicant. Treatment interventions
compared to control conditions reduced the risk of
delivering a low-birthweight infant (RR 0.83, 95% CI
0.730.95) and having a preterm delivery (RR 0.86,
95% CI 0.740.98). Moreover, there were sufcient
studies in the meta-analysis to examine the potential
effectiveness of different types of behavioral interven -
tions. As shown in Table 2, cognitive behavioral
strategies were the most commonly utilized interven-
tion, and resulted in consistently enhanced quit rates.
Contingency management interventions (i.e. reward
type interventions in which participants receive incen-
tives to quit) have achieved the largest increase in quit
rates during pregnancy; however, to date, there are
only four studies of this type of intervention, all
conducted in high-income countries. Although cog-
nitive behavioral strategies are effective in both non-
pregnant and pregnant smokers, contingency man-
agement, which is not consistently effective in non-
pregnant smokers (22), appears to be effective for
cessation during pregnancy (27). Given the
limited number of studies, this type of behavioral
treatment needs further evaluation.
Two studies included in the meta-analysis were
conducted in LMICs. A randomized-controlled trial
Table 2. Effects of interventions on smoking rates during
Number of
risk (95% CI)
Cognitive behavior strategies 30 0.95 (0.93, 0.97)
Stages of change 11 0.99 (0.97, 1.00)
Feedback 4 0.92 (0.84, 1.02)
Rewards (nancial or material) 4 0.76 (0.71, 0.81)
Pharmacotherapy 5 0.95 (0.92, 0.98)
Data based on studies presented in a meta-analysis by
Lumley et al. (27).
446 C.A. Oncken et al.
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conducted in four Latin American cities (Rosario,
Argentina; Pelo tas, Brazil; Havana, Cuba; and
Mexico City, Mexico) examined the impact of a
multi-component home-based health education and
psychosocial support intervention targeting pregnant
women (included education about prenatal smoking)
on knowledge uptake, health behavior change, and
perinatal outcomes (14). Smoking cessation rates did
not increase in the intervention group compared to
the control group; approximately 20% of women in
both groups smoked at study entry and at the end of
In a cluster-randomized trial in the Lodz district of
Poland, the intervention group (n = 205) received four
midwife visits during pregnancy and one after delivery
(20). The control group (n = 181) received standard
written information about the fetal health risks of
maternal smoking. The odds of cessation were sig-
nicantly higher in the intervention than in the control
group (OR 2.5, 95% CI 1.83.7). We did not nd any
other studies examining interventions to decrease
tobacco use during pregnancy in LMICs.
Pharmacotherapy is an integral component of the
treatment of cigarette use and dependence among
non-pregnant women and men in many high-income
countries. Combination of counseling and medica-
tion is more effective than either component alone
(22). To date, seven treatments have been shown to
increase short- and long-term quit rates relative to
placebo, including ve nicotine replacement therapy
(NRT) modalities (gum, patch, nasal spray, inhaler,
and lozenge), bupropion sustained-release (SR), and
varenicline (22). Bupropion is a non-nicotine smok-
ing cessation medication (also used for the treatment
of depression) that may be effective for smoking
cessation by increasing brain levels of dopamine,
norepinephrine, and serotonin (48). It is associated
with a rare risk of seizures, and is contraindicated in
persons with a seizure disorder, or who have anorexia
nervosa or bulimia, or are taking monoamine oxidase
inhibitors (48). Varenicline is a nico tinic receptor
partial agonist specic for the alpha 4 beta 2 receptor
(49). Pharmacotherapy is recommended for cigarette
smokers making a quit attempt if they smoke at least
10 cigarettes per day, are at least 18 years of age, and
are not pregnant (22). A course of pharmacotherapy
typically ranges from six weeks to six months (22)
and rates of success vary with the pharmacotherapy
type, patient withdrawal symptoms, side effect prole,
and perceived helpfulness. Although pharmaco-
therapies are generally considered safe and effective
for smoking cessation, there have been reports of rare
serious neuropsychiatric symptoms (i.e. changes in
behavior, hostility, agitation, depressed mood, sui-
cidal thoughts and behavior, and attempted suici de)
with varenicline and bupropion SR (50).
Pharmacotherapies are not routinely recommended
as rst line treatment for smoking during pregnancy
because safety and efcacy have not been established
for any individual pharmacotherapy (22,51). Animal
studies have shown that nicotine reduces uteropla-
cental blood ow, and has adverse effects on the
developing nervous and pulmonary system (22,52).
Although the risks of nicotine in human pregnancy are
not fully known, based on the adverse effects of
nicotine in animal studies, it seems prude nt to min-
imize the amount of nicotine exposure with NRT if
used during pregnancy (53). Consequently, given the
similar efcacy rates among various NRTs, intermit-
tent replacement therapies (gum or nasal spray) may
be preferable to a continuous nicotine delivery system
because they typically deliver an overall lower dose
with a less constant duration of exposure. The pre-
liminary safety of bupropion has been examined
primarily in observational studies among pregnant
women using this medication for depression or for
smoking cessation. Bupropion SR does not appear to
increase the risk of congenital malformations (54,55).
We did not nd any human studies of the effects of
varenicline use during pregnancy.
Randomized prospective studies have evaluated the
potential utility of pharmacotherapy (nicotine gum,
transdermal nicotine system, nicotine lozenge, bupro-
pion SR) for smoking cessation during pregnancy
(5662). In one meta-analysis, nicotine replacement
was found to have an effect on end of pregnancy quit
rates comparable to cognitive behavioral strategies
(27). In Table 3, we review studies with a sample
size of at least 150, the minimum number to detect
differences in both quit rates and birth outcomes, and
further sub-divide studies based on NRT type and on
whether it was an efcacy or an effectivene ss study.
Two placebo-controlled studies suggest that NRT
does not increase cessation rates, but may increase
birthweight (60,62). Open-label studies have shown
that NRT increases quit rates during pregnancy
(56,61). One study raised concerns about safety
(61); however, baseline differences in race and history
of previous adverse pregnancy outcome between
groups may explain the higher serious adverse event
rate in the NRT group versus the control group (63).
Large placebo-controlled studies examining the
potential safety, tolerability, or efcacy of bupropion
SR or varenicline for smoking cessation during preg-
nancy have not been conducted (54,55,59). More
research is needed to better understand the risk and
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benet prole of each individual pharmacotherapy
for smoking cessation during pregnancy. The risk/
benet proles of an individual pharmacotherapy
cannot necessarily be extrapolated to one another
even within the same class (i.e. gum effects may differ
from patch due to dose and mode of delivery).
Another important consideration is that lack of
availability and cost considerations may prohibit the
use of pharmacotherapies as an integral cessation
component in many LMICs.
Relapse prevention
Unfortunately, the majority of women who are able to
quit smoking during pregnancy relapse after delivery.
A Cochrane review of 54 interventions to prevent
relapse concluded that there was insufcient evi-
dence to support the use of any specic behavioral
intervention to avoid relapse (25). Extended use of
varenicline may help some smokers, and more
research is needed to explore the benet of extended
use of NRT for relapse prevention (25). Of the 14
studies focused on pregnant and postpartum ex-smo-
kers, all of which tested behavioral relapse-prevention
interventions, pooled results of 8 failed to nd any
signicant benet at the end of pregnancy, and 12
failed to nd any benet at follow-up during the
postpartum period (25). Testing of alternative
approaches for effective relapse prevention is needed.
Secondhand smoke exposure
In many LMICs, women (including those who
are pregnant) have low cigarette smoking rates,
but face signicant exposure to SHS at home due
to high smoking rates among men (64). Studies in
high-income countries have shown that policies
that completely eliminate smoking in workplaces
and public places signicantly decrease SHS expo-
sure and improve other health outcomes (65,66).
Increasingly, jurisdictions are banning smoking
in indoor workplaces and in public places. More-
over, the WHO FCTC requires participating
countries to implement measures to protect the
public from indoor SHS exposure in workplaces
and public places, but these measures do not extend
to homes (9).
A Chinese study examined the effect of physician
advice to pregnant women to encourage their hus-
bands to quit smoking in order to limit their SHS
exposure; the intervention included education al
materials on simple strategies to help husbands quit
and brief reminders at subsequent visits (19). Women
receiving this advice reported more quit attempts, a
reduction in cigarettes smoked per day, and a higher
seven-day abstinence rate among their husbands at
the end of treatment. Further research is needed to
determine effective, culturally acceptable interven-
tions to eliminate SHS exposure among pregnant
women, infants, and children in LMICs.
Finally, a Cochrane review found that 11 of 36
identied studies showed a statistically signicant
effect of decreasing childrens SHS exposure in the
intervention versus control groups; 4 of these studies
provided intensive clinical counseling to parental
smokers (67). Of the 36 studies, 5 were conducted
in LMICs (4 in China and 1 in Turkey)
(11,12,15,16,21). Of these 5, 1 was conducted in a
community setting and 4 in pediatric healthcare set-
tings. In 2 of the 4 studies, the parental cessation
intervention was signicantly effective, but 1 of these
2 studies did not biochemically validate quit status.
The review concluded that the current evidence does
not determine which interventions are most effective
for decreasin g parental smoking and preventing
exposure to tobacco smoke in childhood.
Table 3. Studies assessing effectiveness and/or safety of pharmacotherapy use during pregnancy.
Study Design Sample size Study treatment Findings
Wisborg K et al.,
2000 (62)
250 TNS vs. placebo No effect on cessation, birthweight
greater in intervention group
Oncken C et al.,
2008 (60)
194 2 mg nicotine gum vs. placebo No effect on cessation, birthweight
greater in intervention group; risk
of PTD reduced in NRT group
Hegaard HK et al.,
2003 (56)
open label
647 (NRT given to
heavier smokers only)
Choice of NRT (gum, TNS,
both); part of a multi-modal
Increased cessation rates in
intervention group; birthweight
similar between two groups
Pollak KI et al.,
2007 (61)
open label
181 Choice of NRT (gum, TNS, or
Increased quit rates in NRT group;
serious adverse events (mainly
PTD rate) greater in NRT group
Note: NRT, nicotine replacement therapy; PTD, preterm delivery; TNS, transdermal nicotine system.
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As noted earlier, research and implementation of
effective strategies for pregnant women in LMICs
must occur in context with the global tobac co
control efforts of the FCTC and MPOWER strat-
egies. Though the goal of our expert working group
was to set research recommendations, the authors
acknowledge that with the rising global tobac co
epidemic in LMICs, particularly among women,
we are in a time for action, not just research. These
actions must be built on a solid science base.
Therefore, a parallel strategy of quickly developing
effective interventions, while simultaneously evalu-
ating their effectiveness, should be set up as quickly
as possible. This research agenda also aligns with
the Millennium Development Goals to reduce child
mortality and improve maternal health (68).
Considerations for tobacco interventions in LMICs
Few LMICs have data, especially popula tion-
based ones, on the prevalence of tobacco use and
SHS exposure among pregnant women. Addressing
these gaps will help identify the areas where interven-
tions are most urgently needed. Current tobacco
control initiatives should be assessed within a country
before introducing new interventions, to avoid over-
lap and to ensure a comprehensive tobacco control
strategy. Discussions with clinician s, local health
ofcials, and community members may help deter-
mine what interventions would be culturally accept-
able and feasible, and healthc are delivery systems
should be examined to determi ne whether interven-
tions can be integrated into existing frameworks. For
example, two studies in LMICs have incorporated
smoking cessation interventions (e.g. health educa-
tion and counseling) into existing healthcare services
for pregnant women (14,20).
Research and implementation capacity in the
area of tobacco and pregnancy needs to be devel-
oped and enhanced in LMICs. Traditionally, mater-
nal and child health and reproductive health
practitioners have not been trained in delivering
tobacco prevention and cessation interventions.
Efforts should be made to partner when possible
with other tobacco control initiatives within
LMICs, such as the Bloomberg Initiative to reduce
tobacco use, which has provided various capacity
building opportunities and led to a substantial
enhancement in the number of individuals in
tobacco control. These programs, or similar ones,
could be expanded or adapted to treat pregnant
tobacco users.
Recommendations from the expert working group
A working group of international perinatal and
tobacco control experts was convened to rev iew
the summary of the literature search a nd to e stab-
lish research prioritie s in the follo wing areas:
(i) prevent ing the upta ke and reducing tobacc o
use among girls and women of reproductive age;
and (ii) reducing tobacco use and SHS exposure
among pregnant women. To identify research pri-
orities, the working group considered the research
evidence in terms of burden of disease, intervention
impact, intervention costs, feasibility of integration
into existing services, uniqueness of the contribu-
tion, and overall feasibility. The group acknowledged
that interventions tested in high-income countries
may not be directly transferable to LMICs because
of important differences (e.g. smoker demographics,
general awareness of tobacco harms, healthcare
systems); however, the evidence-base provides an
important starting point for research and interven-
tions in LMICs.
Given th at population-level efforts (e.g. increasing
tobacco taxes, prohibiting smoking in public places)
have been shown to have cons istent effects on
decreasing the prevalence of tobacco use, the working
group recommended giving high priority to the fol-
lowing research topics in countries where tobacco use
is becoming more prevalent among women of repro-
ductive age or where a high percentage of women are
exposed to SHS.
Key research priorities
Evaluating the impact of tobacco control policy
efforts on reducing tobacco use and SHS exposure
among pregnant and reproductive age women.
Tobacco control policies include increasing
tobacco taxes, adopting and implementing laws
to eliminate smoking in public places, requiring
health warning messages on tobacco products, and
banning marketing of to bacco products. All of
these policies are required of nations that ratify
the FCTC.
Developing and evaluating cultur ally adapted
interventions that involve brief healthcare provider
advice to quit tobacco use and reduce SHS expo-
sure by pregnant smokers and evaluating whether
psychosocial support, pharmacotherapy, incen-
tives, and addressing other unhealthy behaviors
can provide additional benets. Use of non-
traditional healthcare providers, such as lay health
workers, should also be explored given access to
healthcare systems is often limited in LMICs.
Decreasing tobacco exposure dur ing pregnancy 449
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Evaluating the concurrent implementation of
population-level (e.g. tax increases, smoking
bans) and clinical interventions for cessation
among pregnant and reproductive age women.
The working group determined that the safety and
efcacy of pharmacotherapies during pregnancy
should be assessed in LMICs where pharmacotherapy
is in routine use among non-pregnant smokers.
The working group recommended that reproductive
health outcomes, such as birthweight, gestational age,
placenta previa and abruption, and perinatal and infant
morbidity and mortality, should be evaluated to assess
intervention impact. The working group recom-
mended validating maternal smoking rates with bio-
chemical measurements (i.e. cotinine or exhaled
carbon monoxide measurements) in clinical studies
(69) as high rates of nondisclosure have been consis-
tently documented in high-income countries (70).
Studies without biochemical verication may be
excluded from meta-analyses because of the risk of
bias (27). Measures of quit rates and relapse after
delivery should be assessed for pregnancy-based inter-
ventions. More research is needed on interventions
for the postpartum period as an opportunity to
reduce relapse and increase life-long cessation. Also,
cost-effectiveness studies would provide evidence to
policy-makers that replication and support of these
programs is a wise use of scarce nancial resources.
Finally, some consideration needs to be given to
who should fund interventions to decre ase tobacco
use and exposure among pregnant women. Although
substantial funds have been allotted to improve
maternal and child health globally, very little has
been directed towards decreasing tobacco use and
exposure during pregnancy. Research and interven-
tions should be a key priority for fundi ng agencies
interested in reducing the economic and health effects
of tobacco, and for funding agencies for which
improving maternal and child health is a priority.
In summary, tobacco use is increasing in many
LMICs. In order to prevent high levels of tobacco
use among women in LMICs (similar to many high-
income countries), research is needed to test and
measure the impact of interventions to prevent tobacco
uptake and to aid in cessation in this population. Given
the particular risks for adverse effects on pregnancy and
birth outcomes of tobacco use and SHS exposure,
efforts should be targeted specically to pregnant
women. Studies from high-income countries suggest
that the rate of infant mortality is 40% higher among
pregnant cigarette smokers (71). In LMICs where
infant mortality rates are already high, increased
tobacco use could cause devastating harm. In India,
where womens smokeless tobacco use is common,
there is already a three-fold increased risk of stillbirth
and a two- to three-fold increased risk of having a low
birthweight infant among smokeless tobacco users
(72). Implementation of interventions to prevent or
limit prenatal tobacco exposure and measurement of
the net health benet of such interventions on perinatal
outcomes should be a high priority.
We thank members of the expert working group who
contributed to the discussion of the science and the
development of research priorities on the topic:
Bernardo Agudelo-Jaramillo, MD, GO, Universidad
de Antioqui a, Colombia; Mario Festin, MD, Univer-
sity of the Philippines Manila, Philippines; Mario
Merialdi, MD, PhD, MPH, World Health Organiza-
tion, Switzerland; Patricia Dolan Mullen, DrPH,
University of Texas School of Public Health, USA;
and Katherine Murphy, Medical Research Council,
South Africa.
Participants in the expert meeting entitled Tobacco
exposure during pregnancy in low and middle income
countries: establishing research priorities held 810
September 2008: Bernardo Agudelo-Jaramillo, Erik
Augustson, Cathy Backinger, Dilyara Barzani, José
Belizán, Vincenzo Berghella, John Bernert, Michele
Bloch, Neal Brandes, F. Carol Bruce, Tsungai
Chipato, Sven Cnattingius, Patricia Dietz, Mirjana
Djordjevic, Thomas Eissenberg, Lucinda England,
Ellen Feighery, Mario Festin, Christine Galavotti,
Lorrie Gavin, Robert Goldenberg, Lorraine Greaves,
Prakash Gupta, Paul Holmes, Carys Horgan, Yvonne
Hunt, Ami Hurd, Ann Jensby, Annette Kaufman, Shin
Kim, Priyadarshini Koduri, Michael Kramer, Mats
Lambe, Harry Lando, Xingzhu Liu, Ann Malarcher,
Elizabeth McClure, Mario Merialdi, Suneeta Mittal,
Patricia Dolan Mullen, Katherine Murphy, Mimi
Nichter, Thomas Novotny, Cheryl Oncken, Michael
Paglia, Karen Parker, Alexandra Parks, Zhaoxia Ren,
Jonathan Samet, Susan Sanders, Isabel Scarinci, David
Stamilio, Mary Ellen Stanton, Alan Tita, Jorge Tolosa,
Scott Tomar, Van Tong, Sheela Shenoy Trivikram,
Deborah Winn, and Linda Wright.
Declaration of interest: Dr. Oncken has received
honoraria from Pzer (New York, NY). She has
received at no cost nicotine and/or placebo products
from Glaxo-SmithKline (Philadelphia, PA) and from
Pharmacia & Upjohn (Helsingborg, Sweden) for
research studies. She has received research grant
450 C.A. Oncken et al.
Acta Obstet Gynecol Scand Downloaded from by on 05/20/14
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funding from Pzer and from Nabi Biopharmaceu-
ticals (Boca Raton, FL). Dr. Samet was previously a
member of the Pzer Global Tobacco Advisory
Board. Dr. Bloch has provided depositions on behalf
of the U.S. government in the U.S. Department of
Justice lawsuit, U.S.A. v. Philip Morris USA, Inc.
et al., as part of her ofcial duties. Belizan, Berghella,
Dietz, Goldenberg, Lando, Tolosa, and Tong report
no conicts of interest.
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