October 7, 2008

Tobacco Use and Secondhand Smoke Exposure During Pregnancy: An Investigative Survey of Women in 9 Developing Nations

Objectives. We examined pregnant women's use of cigarettes and other tobacco products and the exposure of pregnant women and their young children to secondhand smoke (SHS) in 9 nations in Latin America, Asia, and Africa. Methods. Face-to-face surveys were administered to 7961 pregnant women (more than 700 per site) between October 2004 and September 2005.

Results. At all Latin American sites, pregnant women commonly reported that they had ever tried cigarette smoking (range: 78.3% [Uruguay] to 35.0% [Guatemala]). The highest levels of current smoking were found in Uruguay (18.3%), Argentina (10.3%), and Brazil (6.1%). Experimentation with smokeless tobacco occurred in the Democratic Republic of the Congo and India; one third of all respondents in Orissa, India, were current smokeless tobacco users. SHS exposure was common: between 91.6%(Pakistan) and 17.1%(Democratic Republic of the Congo) of pregnant women reported that smoking was permitted in their home.

Conclusions. Pregnant women's tobacco use and SHS exposure are current or emerging problems in several low- and middle-income nations, jeopardizing ongoing efforts to improve maternal and child health. (Am J Public Health. 2008;98: 1833-1840. doi:10.2105/ AJPH.2007.117887)

Tobacco use is widely recognized as one of the leading threats to global health.1 Historically, the prevalence of smoking among women in the developing world has been very low, in part because of strong cultural constraints against women's smoking; approximately 50% of men in developing nations smoke cigarettes, compared with 9% of women.2 Averting an increase in the prevalence of smoking among women in developing nations is widely recognized as a signifi- cant public health opportunity.3,4

Pregnant women are a priority population for tobacco control efforts because both cigarette smoking and smokeless tobacco use during pregnancy pose serious risks to fetal health. Smoking during pregnancy may cause preterm delivery, low birthweight, and sudden infant death syndrome; smokeless tobacco use during pregnancy has been associated with stillbirth, preterm birth, and reduced birthweight.5-8 Maternal tobacco use is also likely to expose infants and children to secondhand smoke (SHS) and to provide a role model for children's use of tobacco. Intervening during pregnancy is also important because of the health risks to the woman, who potentially has many years of remaining life. For cigarette smoking, these health risks include lung and other cancers, coronary heart disease and stroke, and chronic obstructive pulmonary disease; health risks from smokeless tobacco products include oral and pancreatic cancer.9,10

The US National Institute of Child Health and Human Development's Global Network for Women's and Children's Health Research consists of 10 research units chosen for scientific merit that are focused on improving maternal and children's health in the developing world. To determine whether pregnant women's tobacco use and SHS exposure are emerging public health issues, the Global Network undertook an investigative survey of pregnant women's knowledge, attitudes, and behaviors regarding tobacco use and SHS exposure. Here we report findings on pregnant women's experimentation with and use of tobacco products, their perceptions of the social acceptability of tobacco use by women, and their and their young children's exposure to SHS.


We conducted a multicenter, cross-sectional survey of a convenience sample of pregnant women in 9 research units of the Global Network. The participating research units worked with pregnant women at study sites in Latin America (Argentina, Brazil, Ecuador, Guatemala, and Uruguay), Africa (Democratic Republic of the Congo [DRC] and Zambia), and Asia (Pakistan and 2 states in India). The number and location of recruitment sites for each research unit are shown in Table 1.

Questionnaire Design

The questionnaire was designed for faceto- face verbal administration by trained interviewers. Where possible, we used items from preexisting surveys, such as the Global Youth Tobacco Survey,11 the 2000 US National Health Interview Survey,12 and the Smoke- Free Families Screening Form,13 to develop the questionnaire. Survey topics included pregnant women's use of tobacco products, knowledge of health hazards, perception of the social acceptability of tobacco use by women, and exposure to advertising both for and against tobacco and pregnant women's and children's SHS exposure.

The research team in each country translated the master English version of the questionnaire into the language or languages most commonly spoken by the intended respondents. A back-translation was compared with the original English version, and discrepancies were returned to the sites for resolution. Each participating site conducted a pretest of the questionnaire with approximately 20 pregnant women drawn from the target population of the main survey. The final version of the questionnaire required an average of 25 minutes to administer across all sites. Interviewers were selected by the site team and included physicians, nurses, medical and nursing students, and other health professionals. Data were collected between October 2004 and September 2005. Response rates were between 97.7% and 100%.

Determination of cigarette smoking and other tobacco use status. All respondents were asked, "Have you ever tried cigarette smoking, even 1 or 2 puffs?" and those responding "yes" were considered to have ever experimented with cigarettes. Those who had ever experimented with cigarettes were asked if they had ever smoked daily and if they had smoked 100 cigarettes or more in their lifetime. Respondents who answered "yes" to either or both questions were considered to have ever been a regular cigarette smoker. Respondents who had ever been a regular cigarette smoker and those who had ever experimented with cigarettes were then asked about their current smoking. Those who acknowledged they were currently smoking were considered current smokers.

Similarly, all respondents were asked if they had ever tried 'any other forms of tobacco, besides cigarettes?" and those responding "yes" were considered to have ever experimented with any other tobacco product. Respondents who had ever experimented were queried separately about each product for up to 4 other tobacco products; they were asked if they had ever used the product daily and if they had used the product 100 or more times in their lifetime. Respondents who answered "yes" to either or both questions were considered to have ever been a regular user of that product. Respondents who had ever been a regular user and those who had ever experimented were asked about their current use. Those who acknowledged they were currently using the product were considered current users.

Determination of exposure of women and their young children to secondhand smoke. All respondents were asked, "Is smoking of tobacco products allowed in your home?" All respondents were also asked, "How often are you indoors and around people who are smoking cigarettes or other types of tobacco products?" and "How often are your children, 5 years or younger, indoors and around people who are smoking cigarettes or other types of tobacco products?" Permitted responses to the latter 2 questions were rarely or never, sometimes, frequently, or always.

Determination of perceived acceptability of women's tobacco use. All respondents were asked, "Do you think it is acceptable for women in your community to smoke cigarettes, or not?" and "Do you think it is acceptable for women in your community to use other tobacco products, or not?"

Questionnaire Administration

Sample population, inclusion criteria, and informed consent. Each research site administered the questionnaire to a convenience sample of 700 or more pregnant women (N=7961) presenting for prenatal care. Participants were identified at prenatal care clinics, hospitals, health centers, and in Orissa, India, community sites accessible to the research team. Eligibility requirements included being aged 18 to 46 years and being beyond the first trimester of pregnancy. Women believed to be mentally or physically incapable of participating in the survey, as judged by the interviewer, were excluded. We obtained written consent from all willing, eligible women, except in Pakistan and Ecuador, where verbal consent was permitted. Respondents did not receive incentives or reimbursement for their participation. Interviews were conducted with the maximum privacy possible in each setting.

Quality control. Standard procedures, established to ensure data quality, included training programs for the interviewers, supervisors, and data-entry staff; a reporting system to monitor data collection and processing activities; and procedures for verifying interviewers' work. The in-country research team conducted interviewer training, with materials and supervision provided by the data coordinating center, Research Triangle Institute. Trainees completed a certification test to determine whether they were prepared to solicit participation in the study and administer the questionnaire or they needed additional training. For each interviewer, supervisory staff recontacted a 5% to 10% sample of participants to verify that the interview occurred and to confirm key data. A data management system developed for each site included data-entry range and intraform consistency checks (e.g., skip patterns) to ensure high-quality keying. Staff selected a 10% sample of completed questionnaires for key verification. We reviewed any verification exercise with an error rate of greater than 0.5% to identify the source of error and correct the problem. An Internet- based field-monitoring system tracked progress in each country.

Sample size estimation and statistical methods. Each site set a target sample of 750 completed interviews to estimate parameters of knowledge, attitudes, and behaviors as low as 0.05 with a coefficient of variation of about 15%. Staff entered data into a data management system developed with Microsoft Access 2002 (Microsoft Corp, Redmond, Wash). Data were reviewed for consistency and completeness at the data coordinating center. Questionnaires with incomplete or inconsistent information were returned to the sites for resolution. We used SAS version 9.0 (SAS Institute Inc, Cary, NC) for data analysis. We calculated descriptive statistics (frequencies, percentages, means, and standard deviations) for each site, excluding missing data from the analysis.


Respondents were primarily from rural areas in Pakistan and India; urban areas in Argentina, Uruguay, Brazil, and Zambia; and a mixture of settings at the remaining sites (Table 1). At most sites, the respondents' mean age was mid-20s. Very high literacy levels (>95%) were found at all Latin American sites and intermediate literacy levels (59.3%-90.8%) at the African and Indian sites. Fewer than 1 in 4 pregnant women surveyed at the site in Pakistan were literate. At all sites, most respondents were either married or a member of a couple; the majority did not work for pay. The 2 Indian sites had the highest percentages of women who reported living with at least 1 household member who used a tobacco product (90.4% in Orissa; 83.0% in Karnataka). In Argentina, Uruguay, and Pakistan, 56.1% to 59.7% of respondents reported living with at least 1 household member who used a tobacco product; at the remaining sites, this percentage was lower. Except at the sites in Orissa and Ecuador, less than 5% of respondents had a household member who was involved in the growth, manufacture, or sale of tobacco.

We found striking differences in respondents' cigarette smoking behaviors (Table 2). Levels of having ever experimented with cigarettes were high throughout Latin America, especially at the sites in Uruguay (78.3%), Argentina (75.3%), and Ecuador (57.6%). The level of cigarette experimentation in the DRC (14.1%) was more than double that of Zambia (6.6%). Negligible rates of experimentation were found at both Indian sites, but 1 in 10 respondents at the site in Pakistan had experimented with cigarettes.

The sites in Uruguay and Argentina had the highest percentage of pregnant women who had ever been a regular cigarette smoker (53.0% and 44.3%, respectively). Fewer pregnant women had ever been regular smokers at the sites in Brazil (20.6%), Guatemala (10.4%), Ecuador (4.3%), and Pakistan (3.2%). We found striking differences between sites in the percentage of pregnant women who had transitioned from experimentation to regular cigarette use. Fewer than 10% of pregnant women who had ever tried cigarette smoking had ever transitioned to regular use at the sites in the DRC, Zambia, and Ecuador, in contrast to much higher percentages in Uruguay (67.7%), Argentina (58.9%), Brazil (45.8%), Pakistan (31.0%) and Guatemala (29.7%).

At all Latin American sites, the majority of pregnant women who had ever been regular cigarette smokers reported that they were not currently smoking; however, levels of current smoking were 18.3% in Uruguay, 10.3% in Argentina, and 6.1% in Brazil. Although very few pregnant women at the site in Pakistan had ever smoked regularly, 76.9% of these reported they were currently smoking. Respondents in Argentina, Uruguay, and Brazil were far more likely than were those at other sites to believe that cigarette smoking was acceptable for women.

The highest percentage of respondents who had ever tried any other (noncigarette) tobacco product were in the DRC (41.8%), Orissa (34.2%), and Karnataka (9.0%; Table 3). At all other sites, this figure was below 5% (data not shown). Pregnant women at both Indian sites reported using either chewing tobacco or tobacco tooth powder or both, whereas those in the DRC reported using snuff or chewing tobacco. At both Indian sites, most (more than 85%) of those who had ever experimented with any other tobacco product had transitioned to regular use, and a majority were also current users (98.3% in Orissa; 58.6% in Karnataka). In the DRC, almost no pregnant women had ever been regular users of other tobacco products; however, 6% were currently using any other tobacco product during pregnancy. The percentage of respondents who believed that the use of other tobacco products was acceptable for women was highest in Karnataka (44.4%).

Many pregnant women reported that smoking cigarettes or other tobacco products was permitted in their home, including more than 90% of respondents at the site in Pakistan and more than half in Orissa, Argentina, and Uruguay (Table 4). In Pakistan, nearly half (49.9%) the respondents reported that they were frequently or always exposed to tobacco smoke indoors, and 51.4% reported that their young children were frequently or always exposed to tobacco smoke indoors. Pregnant women's and young children's exposure was also common at some other sites; more than 25% of pregnant women were frequently or always exposed to tobacco smoke indoors in Argentina, Uruguay, and Brazil, and more than 15% of young children were frequently or always exposed to tobacco smoke indoors in Brazil, Uruguay, and Karnataka.


To our knowledge, our study was the first to examine pregnant women's tobacco use, SHS exposure, and attitudes toward women's tobacco use in multiple developing (i.e., lowand middle-income) countries.14 Our results provide evidence that pregnant women's cigarette smoking is a current or emerging problem in the 5 Latin American nations surveyed. Indeed, the sites in Argentina and Uruguay recorded the highest levels of cigarette use among pregnant women at any of the 10 sites. Although the other Latin American sites had far fewer pregnant women who had ever been regular smokers, all had far more respondents who reported they had ever tried cigarettes. Experimentation with cigarettes is an early and important step toward becoming a regular smoker.15-17 Should barriers to continuing past experimentation be lifted, these sites would be poised for much higher levels of female cigarette smoking. Other evidence also indicates that parts of Latin America are experiencing high levels of female tobacco use.2,18

The study also provides evidence that pregnant women's experimentation, regular use, and use during pregnancy of smokeless tobacco products is of concern in the 2 Indian states surveyed. This was particularly true in Orissa, where one third of all pregnant women surveyed were currently using some form of smokeless tobacco. Tobacco consumption in India involves diverse tobacco products and is thought to be increasing by 2% to 3% per year.19 Subramanian et al. estimated that nationwide, 3.4% of Indian women smoked tobacco, 13.0% chewed tobacco, and 15.5% both smoked and chewed tobacco; they found wide variation in the prevalence of tobacco use between different states.20

Four in 10 respondents from the DRC had ever tried smokeless tobacco; preliminary evidence suggests that DRC respondents viewed snuff and chewing tobacco as forms of medicine or used these products for their pharmacologic effects or as an alternative to alcohol. Of the 6 regions designated by the World Health Organization, the African region has the largest number of countries that lack information on smoking prevalence; however, available evidence suggests that most African nations are in the early stages of the tobacco epidemic.21 Consistent with this view, an analysis of the Demographic Health Surveys for Malawi (2000) and Zambia (2001- 2002) found very few female cigarette smokers in either country.22

Smoking by others in the household can pose a serious threat to maternal and child health. SHS is a human carcinogen that causes lung cancer and heart disease in adults, and serious illnesses, such as bronchitis and pneumonia, in infants and children. 23-25 In addition, SHS may add to the other respiratory burdens commonly found in developing nations, including exposure to smoke from burning solid fuels and, in urban areas, high levels of air pollution.26,27 Many of the pregnant women surveyed lived with at least 1 tobacco user; these women may find it difficult to prohibit smoking in their homes, given the lower social status of women in many countries.28

Recent work has linked smoking to health risks of particular concern in developing nations. A systematic review and meta- analysis concluded that active smoking is associated with an increased risk of tuberculosis, and some evidence that SHS exposure may also increase tuberculosis risk was found.29 Smoking may be an independent risk factor for HIV infection, it further compromises the health status of HIV-infected individuals, and it has been associated with decreased effectiveness of highly active antiretroviral therapy.30-32 Of particular concern for poor families in developing nations is the fact that expenditures on tobacco products compete with household spending on food, health care, and other basic resources.33,34 Finally, compared with women and newborns in developed nations, complications of pregnancy caused by tobacco use pose a far greater threat to women and newborns in developing nations, where access to skilled professional care during and after labor and delivery is frequently lacking.35 These data highlight the urgent need to implement evidence-based interventions to prevent and control tobacco use among pregnant women.36-38 The Framework Convention on Tobacco Control, a landmark treaty that focuses on implementing evidence-based interventions, such as price and tax measures to reduce the demand for tobacco, and comprehensive bans on advertising, promotion, and sponsorship of tobacco products, explicitly recognizes the threat of increased tobacco consumption by women and young girls worldwide.39 In addition, the Bloomberg global initiative is aimed at helping low- and middle-income nations to adopt proven tobacco control measures.40

Interventions targeting women will benefit from a life-span approach, rather than from a narrow focus on pregnancy alone. Preventing tobacco use by girls and young women is arguably the single most effective way to prevent tobacco use during pregnancy. Experience from the developed world demonstrates that many women quit smoking during pregnancy, only to relapse after delivery.41 Greaves et al. highlight the need to understand and address structural factors, such as poverty and social class, that are barriers to women's abstinence from tobacco.42 Finally, Lambert argues that tobacco control for women (and men) is "not only a matter of public health but also a matter of fundamental human rights," noting that several key international agreements have established that women, like men, have the "right to health."43(p32)

Between 1970 and 1998, tobacco consumption in developed nations declined by about 0.2% annually, and consumption in developing countries increased by about 3.1% annually, primarily because of population and income growth; by 2010, developing nations will account for approximately 70% of global tobacco consumption.44 In 2003, the Global Youth Tobacco Survey reported little difference between boys' and girls' tobacco use; the authors noted that this finding underscored the potential growth of the tobacco epidemic among women in developing nations, where most of the study sites were located. 45 Lopez et al. have put forth a widely used 4-stage model of cigarette smoking in developed countries, which emphasizes the 3- to 4-decade lag between the peak in mortality caused by tobacco use and the peak in national smoking prevalence and also helps explain the patterns of tobacco use now being seen in developing nations, such as those found in our study.46

Our study had several recognized limitations. Data were collected by self-report in face-to-face interviews. Tobacco use by women, especially pregnant women, is heavily stigmatized; our findings may well have underestimated the scope of the problem if respondents were reluctant to acknowledge their tobacco use. The study was limited to pregnant women aged 18 to 46 years; the findings cannot necessarily be generalized to nonpregnant women in this age group, nor to adolescent girls or older women. Each site surveyed a convenience sample of pregnant women because resource constraints did not permit us to collect data from a nationally representative sample. Besides residing in different countries, respondents differed in other ways that may have contributed to the differences observed, including geographic setting, literacy levels, employment status, and the presence of tobacco users in the household.

In most developing nations, cultural norms have tended to severely limit tobacco use by women, including pregnant women.47,48 Similar norms were present in many developed nations, including the United States, during the early 20th century, but they eroded over time, in part because of tobacco industry marketing efforts directed at women.49-51 As use has declined in the developed world, tobacco companies have increased their promotional efforts in the developing world.52,53 Today, a key challenge is to contain women's tobacco use in low- and middle-income nations as women's status improves and traditional barriers to their tobacco use erode.

Public health efforts to improve maternal and child health date back to the early 20th century.54 The Millennium Development Goals explicitly recognize the importance of improving maternal and child health as a means to increase economic development, and unprecedented new resources are being devoted to improving global health.55,56 Ironically, these efforts are occurring at a time when rising tobacco use in the developing world threatens to impede or reverse hardwon global health gains. In particular, pregnant women's tobacco use and exposure of pregnant women and their young children to SHS jeopardize efforts to improve maternal and child health in developing nations. However, if prompt and vigorous actions are taken, it should be possible to avert an epidemic of tobacco use among pregnant women in developing countries, who are among the world's most vulnerable citizens.


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Michele Bloch, MD, PhD, Fernando Althabe, MD, MSc, Marie Onyamboko, MD, MPH, Christine Kaseba-Sata, MBChB, DGO, MRCOG, Eduardo E. Castilla, MD, PhD, Salvio Freire, MD, Ana L. Garces, MD, MPH, Sailajanandan Parida, MD, Shivaprasad S. Goudar, MD, MHPE, Muhammad Masood Kadir, MBBS, MPH, FCPS, Norman Goco, MHS, Jutta Thornberry, BA, Magdalena Daniels, AD, Janet Bartz, MS, Tyler Hartwell, PhD, Nancy Moss, PhD, and Robert Goldenberg, MD

About the Authors

At the time of the study, Michele Bloch was with the National Cancer Institute, National Institutes of Health, Bethesda, MD. Nancy Moss was with the National Institute of Child Health and Human Development, National Institutes of Health, Bethesda. Fernando Althabe is with the Hospital de Clinicas, Montevideo, Uruguay. Marie Onyamboko is with the Kinshasa School of Public Health, University of Kinshasa, Kinshasa, Democratic Republic of the Congo. Christine Kaseba-Sata is with the University Teaching Hospital, Lusaka, Zambia. Eduardo E. Castilla is with the Estudio Colaborativo Latinoamericano de Malformaciones Congenitas (Latin-American Collaborative Study of Congenital Malformations), Rio de Janeiro, Brazil. Salvio Freire is with the Hospital das Clinicas, Federal University of Pernambuco, Recife-Pernambuco, Brazil. Ana L. Garces is with the Multidisciplinary Health Institute, Guatemala City, Guatemala. Sailajanandan Parida is with the Sriram Chandra Bhanj Medical College, Cuttack, India. Shivaprasad S. Goudar is with the Karnatak Lingayat Education Society's Jawaharlal Nehru Medical College, Belgaum, India. Muhammad Masood Kadir is with the Aga Khan University, Karachi, Pakistan. Norman Goco, Jutta Thornberry, Magdalena Daniels, Janet Bartz, and Tyler Hartwell are with Research Triangle Institute, Research Triangle Park, NC. Robert Goldenberg is with Drexel University College of Medicine, Philadelphia, PA.

Requests for reprints should be sent to Michele Bloch, Tobacco Control Research Branch, National Cancer Institute, Executive Plaza North, Room 4038, 6130 Executive Blvd, MSC 7337, Bethesda, MD 20892- 7337 (email: [email protected]).

This article was accepted August 27, 2007.


M. Bloch led the study, participated in and oversaw all aspects of the research, and took major responsibility for writing the article. F. Althabe, M. Onyamboko, C. Kaseba-Sata, E.E. Castilla, S. Freire, A.L. Garces, S. Parida, S.S. Goudar, and M.M. Kadir obtained local ethics board approvals; contributed to the study design, protocol, and questionnaire development; supervised field staff training; oversaw data collection, entry, and transmission; assisted in data cleaning and analysis; and reviewed the article. N. Goco contributed to the development of the protocol and questionnaire, coordinated the development and implementation of the survey and the monitoring of data collection, and contributed to the article. J. Thornberry led questionnaire and training material development, conducted remote training of site supervisors on data collection implementation, and contributed to the article. M. Daniels developed the data management system, supervised data entry and transmission, and contributed to the article. J. Bartz led data cleaning, performed statistical analyses, and contributed to the article. T. Hartwell oversaw development of the survey design and protocol, served as lead statistician, and contributed to the article. N. Moss contributed to oversight of the study, including survey development and implementation, field training, and data analysis, and helped write the article. R. Goldenberg contributed to the development of the study design, protocol, and questionnaire and helped edit the article.


Financial support for this research was provided by the National Institute of Child Health and Human Development and the National Cancer Institute, US National Institutes of Health; the US Department of Health and Human Services' Office on Women's Health; and the Bill and Melinda Gates Foundation. (grant numbers U01- HD40477, U01-HD43475, U01-HD43464, U01-HD40561, U01-HD40565, U01- HD40657, U01-HD40574, U01-HD42372, U01-HD40607, U01-HD40636).

We are grateful to the women who participated in the survey and the field staff from each country for making this research possible. We also thank Gary Giovino, Linda Pederson, and Corinne Husten for their helpful comments on the questionnaire.

Human Participant Protection

The study protocol, consent form, and questionnaire were approved by institutional review boards at the data coordinating center, Research Triangle Institute, the US-based institutions, and the local collaborating institutions at each site.

Copyright American Public Health Association Oct 2008

Originally published by Bloch, Michele Althabe, Fernando; Onyamboko, Marie; Kaseba-Sata, Christine; Castilla, Eduardo E; Freire, Salvio; Garces, Ana L; Parida, Sailajanandan; Goudar, Shivaprasad S; Kadir, Muhammad Masood; Goco, Norman; Thornberry, Jutta; Daniels, Magdalena; Bartz, Janet.

(c) 2008 American Journal of Public Health. Provided by ProQuest LLC. All rights Reserved.