Open-access Smoking and its peculiarities during pregnancy: a critical review

Abstracts

Pregnancy presents a special opportunity to promote smoking cessation. Concern for the health of the fetus can be extraordinarily motivating for the pregnant woman. Results and cost-effectiveness of antismoking interventions are better for this group than for the general population, and the advantages exceed the benefits to the health of the mother alone, since they also allow for the development of a healthy fetus. Knowledge of the peculiarities of smoking during pregnancy is fundamental to developing a directed approach, which increases the probability of success. This review investigates the extent of the harmful effects that smoking has on pregnant women and fetuses alike and advocates the use of appropriate techniques to encourage pregnant women to stop smoking.

Smoking; Smoking cessation; Pregnancy


A gestação é uma ocasião especial para a promoção da cessação do tabagismo. A preocupação com a saúde do feto gera uma motivação extraordinária na gestante. Os resultados e a relação custo-efetividade das intervenções são melhores neste grupo do que na população em geral. Os ganhos extrapolam os benefícios à saúde da mulher, pois permitem também o desenvolvimento de um feto mais saudável. O conhecimento das peculiaridades do tabagismo durante a gestação é fundamental para uma abordagem direcionada e com maior probabilidade de sucesso. Este trabalho de revisão tem o objetivo de ressaltar a extensão dos malefícios do fumo, tanto para a mulher gestante quanto para seu feto, e estimular o uso de técnicas apropriadas para a suspensão do tabagismo nesta população.

Tabagismo; Abandono do uso de tabaco; Gravidez


REVIEW ARTICLE

Smoking and its peculiarities during pregnancy: a critical review *

Waldir Leopércio; Analice Gigliotti

Correspondence Correspondence Waldir Leopércio Rua Conde de Irajá, 420 Rio de Janeiro, Brasil Cep: 22271-020 Phone/fax: (21) 2535-5910 e-mail: cdtorax@terra.com.br

Pregnancy is a special occasion to promote the end of the smoking habit. Concern with health of the fetus brings about an extraordinary motivation for the pregnant woman. Results and cost-effectiveness of interventions are better in this group than in the overall population and the advantages extrapolate the benefits to the woman™s health as they also allow for the development of a healthy fetus. Knowledge of the peculiarities of smoking during pregnancy is fundamental for a directed approach which adds to a probability of greater success. This review investigates the extent of the harm of tobacco for the pregnant woman as well as for the fetus. As such it, it encourages the use of appropriate techniques to urge pregnant women to stop smoking.

Key words: Smoking/adverse effects. Tobacco use cessation/methods. Pregnancy.

Introduction

Smoking during pregnancy has implications that go beyond the prejudicial effects on maternal health. The adverse effects on fetal health are innumerable, justifying the comment often made by health personnel: that such fetuses are truly “active smokers”.

Smoking by pregnant women is responsible for 20% of cases of low birth weight, 8% of all preterm deliveries and 5% of all perinatal deaths.1 Studies reveal that smoking during pregnancy may contribute to sudden infant death syndrome (SIDS) as well as to significant changes in the development of the fetal nervous system.2 Economic estimates indicate that the costs of perinatal complications are 66% higher for women who smoked during pregnancy than for those who did not.3 Although the fetus will obviously benefit most if the mother stops smoking at the beginning of gestation,4 cessation at any moment during pregnancy, or even during the post-natal period, has a significant impact on the family health. Approximately 27% of American children are exposed to second-hand smoke in the home,5 and annual medical costs of parental smoking are estimated at 4.6 billion USD.6 Maintenance of smoking cessation during gestation and the postpartum period plays a fundamental role in preventing smoking-related diseases that affect the health of both the mother and the child.

The health benefits for mothers, fetuses and young children, as well as the extraordinary motivation for smoking cessation that pregnancy itself provides, justify the adoption of special programs to encourage smoking cessation among pregnant women. Within this context, the objective of this study is to critically review the most important national and international studies on the smoking habit and its effects during pregnancy. Only those articles published in 2003 were considered and all articles were accessed via the Medical Literature, Analysis, and Retrieval System Online (MEDLINE) database or the Literatura Latinoamericana y del Caribe en Ciencias de la Salud (LILACS) database.

Toxicity of tobacco and its effects on fetuses and pregnant women

Nicotine

Placental insufficiency has been incriminated as the main mechanism for fetal growth retardation in pregnant women who smoke. Nicotine causes uterine and placental vasoconstriction, reducing blood flow and the amount of oxygen and nutrients received by the fetus. However, some authors2,7 believe that cellular and molecular damage caused by carbon monoxide and other toxins also significantly interferes with fetal development.

Prenatal and perinatal exposure to nicotine has been associated with cognitive changes,8 impaired psychomotor development9 and gender-dependent biological changes10 in children. These effects seem to be secondary to neurotoxicity induced by nicotine, which interacts with nicotinic cholinergic receptors, still in their early, insufficient stage during pregnancy, and has a negative effect on neurogenesis and synaptogenesis.11

The exact cause of sudden infant death syndrome (SIDS) is still unknown and is probably multifactorial. Smoking during pregnancy is recognized as a risk factor for SIDS. One of the hypotheses regarding this relationship is that prolonged nicotine exposure causes changes in the fetal adrenal medulla, leading to loss of hypoxia tolerance.13 Therefore, during apnea or airway obstruction in newborns, there is no catecholamine secretion to promote redirection of blood flow to the brain and heart or maintenance of the heart rate during hypoxia.

Gilliland et al. reported that fetal exposure to chemicals found in tobacco smoke affects lung development and causes a reduction in the small airways, resulting in altered respiratory function, beginning in childhood and persisting into adulthood.14,15 Changes in lung development may increase the risk for developing chronic obstructive pulmonary disease (COPD), lung cancer or cardiovascular disease later in life.16-18

Nicotine causes sudden, momentary changes in the cardiovascular system of a pregnant woman, together with increased heart rate and higher arterial systolic and diastolic pressure. These changes are dose-dependent and do not seem to have significant repercussions on the health of mother or the fetus.19

Carbon monoxide

Carbon monoxide is a poisonous gas produced by the incomplete burning of organic material. Although there are other sources of exposure to carbon monoxide, such as air pollution, second-hand smoke, endogenous production, and occupational exposure, nothing compares to active smoking.20

Carbon monoxide binds to maternal and fetal hemoglobin 200 times more readily than does oxygen,21 producing carboxyhemoglobin (COHb). The elimination half-life of COHb ranges from 5 to 6 hours,22 and its concentration in the blood of smokers ranges from 5% to 10%. Fetal hemoglobin binds more strongly to carbon monoxide than maternal hemoglobin does, which results in higher levels of COHb in fetal circulation.23 Higher concentrations of COHb cause tissue hypoxia, stimulating erythropoiesis and provoking elevated levels of hematocrit in pregnant smokers and their fetuses.24 This results in blood hyperviscosity, higher risk for infarction in the newborn brain,25 and poor placental function.26

Carbon monoxide alters the oxyhemoglobin dissociation curve – to the detriment of tissue oxygenation.23 Chronic cellular hypoxia is one of the factors that may be implicated in fetal growth retardation.7

Carbon monoxide acts as a potent toxin in the nervous system of the fetus and may cause temporary or permanent brain lesions,27 as well as increasing the heart rate and causing myocardial hypertrophy.28

Other toxic effects of chemicals found in cigarette smoke

It is known that smoking affects the immune system, reducing the phagocytic capacity of macrophages and altering the IgA level in mucous membranes.29 This may explain why pregnant smokers are more likely to have miscarriages.30 Preterm premature rupture of fetal membranes may be caused by focal rupture,31 which is in turn caused by local infection fomented by the toxic substances in tobacco smoke.

Another important cause of premature rupture of the membranes and subsequent miscarriage in smokers is the up to 50% reduction in concentrations of ascorbic acid (vitamin C) in amniotic fluid compared to nonsmokers.32 In addition to playing an important role in the immune defense system,33 vitamin C is essential for the production of collagen, of which the amniochorionic membrane is composed.34 Furthermore, amino-acid transport is decreased in smokers,35 interfering with protein synthesis and thereby also contributing to the poor development of the amniochorionic membrane.36

Another factor responsible for a larger number of miscarriages in smokers is the decrease in placental synthesis of nitric oxide, a potent relaxant of the myometrium.37

Through prostaglandin synthesis, platelet-activating factor is involved throughout the labor process. Smoking reduces the inactivation of this factor, which can cause uterine contraction and preterm delivery.37

Biochemical determination of smoking status in pregnant women

Social pressure and knowledge on the harmful effects of smoking on maternal and fetal health make pregnant women reluctant to accurately report their smoking habits.38 Therefore, the determination of smoking status is important, especially in epidemiological exams and scientific research.39

Today, the indiscriminate use of biochemical confirmation of self-reported smoking status has been questioned.40 Its importance is directly related to the characteristics of the population in study.41 When there is a high chance of false reporting, as in the case of pregnant women, the credibility of data gathered through self-reporting should be verified. Studies on smoking habits during pregnancy may present discrepancies ranging from 28% to 50% between self-reported smoking levels and cotinine levels.42

In studies of pregnant women, verification methods may vary depending on the type of information sought. Today, the most common methods involve determination of expired carbon monoxide (CO) levels or of cotinine levels in urine or saliva. Each method has its own unique characteristics.

If the objective is to determine the smoking status of pregnant women (to differentiate between smokers and nonsmokers), measurement of cotinine levels is the method of choice, despite its technical complexity. However, determination of expired CO levels is a rapid way of evaluating passive smoking or confirming changes in the number of cigarettes smoked and can increase the motivation for a change in behavior.43,44

Critical evaluation of costs in smoking control during pregnancy

Expenditures incurred during pregnancy as a result of smoking by pregnant women represent only a portion of the overall cost of related specialty care services required smoking. Newborns and infants become victims of the smoking habits of their mothers during gestation, breastfeeding and development and therefore require special care, especially in their first year of life.

In the USA, the costs related to obstetrical emergencies attributable to smoking during pregnancy range from 135 to 167 million USD per year.45

Economic estimates indicate that direct medical costs of perinatal complications for pregnant smokers are 66% higher than for nonsmokers.46 This is mainly due to fetal complications, such as low birth weight (LBW),47 which, according to the World Health Organization (WHO), is the most significant isolated risk factor for infant morbidity and mortality48 related to SIDS,12,49 respiratory distress syndrome,14,15 and other conditions.49

In developing countries, smoking during pregnancy is, together with maternal malnutrition and lack of prenatal assistance, the principal cause of LBW.47 In developed pockets within such countries as well as in industrialized nations, it is the main isolated cause.50

In a study published in the journal Health Economics, Adams et al.51 state that smoking during pregnancy increases the risk of neonatal ICU admission by 20%. The authors go on to report that that hospital stays are longer and neonatal ICU costs higher for these infants than for those whose mothers did not smoke during pregnancy. They conclude that smoking during pregnancy increases the cost of neonatal assistance by an average of 700 USD per case.

Smoking during the first year of the life of the child aggravates the respiratory, neurological, and psychomotor damage that began during intrauterine life,14,52 increasing the cost of giving medical care to the children of smokers.

Based on the medical definition of the term “cost-effective”, as put forth by by Doubilet et al.,53 in order to determine the cost-benefit relationship of a health program, it is necessary to evaluate the extent to which the program both improves health care and reduces costs. Alternately, health care delivery may be considered in terms of acceptable costs. Programs for prevention and treatment of smoking present the best cost-benefit relationship among all strategies for health promotion. when compared to any other preventive programs in isolation, antismoking programs also have the greatest impact on life expectancy.54 The World Bank assures that investing in programs to prevent smoking and promote smoking cessation are highly profitable, especially for developing countries.55

When we consider antismoking programs for pregnant women, the cost-benefit relationship is maximized. The benefits obtained from smoking cessation affect not only the health of the expectant mother, but also of the fetus and the family. If a pregnant woman quits smoking by the twentieth week of pregnancy, her risk of having an LBW baby is equal to that of a nonsmoker.56 Awareness of pregnancy is, in itself, an additional motivating factor for smoking cessation. The most opportune time to encourage pregnant women to stop smoking or discourage them from reinitiating the habit is during prenatal visits, which offer many opportunities for reinforcing the antismoking interventions, thereby improving the chances of success.57 Smoking cessation program success rates are approximately three times higher in pregnant women than in any other group.58 Government officials and health administrators are motivated to invest in such programs by the fact that the return on the investment is prompt and easily measured, since the benefits for the health of both mother and newborn (and the consequent savings) can be calculated at the end of gestation.

Every dollar spent on smoking cessation during pregnancy could save approximately 6 dollars in perinatal costs, or up to 17 dollars if we consider the total savings during the first year of life.50,59 Even so, in countries such as the USA and Canada, where antismoking governmental policies are aggressive against smoking during pregnancy, there is still much to be done. Approximately 20% of American60 and 24% of Canadian61 women continue to smoke during pregnancy. Only 49% of obstetricians warn their patients of the consequences of smoking, and only 28% discuss smoking cessation strategies with patients.62

A study carried out in public and private prenatal care institutions in California (USA) showed that 8% of institutions offer no assistance for smoking cessation,63 and only 45% of managed care plans provide information regarding the standard recommendations for pregnant women set forth by the Agency for Health Care Policy and Research.64

Although data from the USA cannot exactly be superimposed on data from Brazil, we can infer that our reality is similar to or even worse than theirs. Smoking by pregnant Brazilian women also affects thousands of lives and costs millions of Brazilian reals that could be used, for example, to improve prenatal care and reduce the infant mortality rate.

Prevention and treatment of smoking behavior during pregnancy

Education and training in antismoking strategies for health professionals, as well as implementation of public and private programs to promote and support smoking cessation, have been extremely efficient in reducing smoking among pregnant women.38,42,65

The prevalence of smoking among pregnant American women is higher among the young (less than 20 years of age)66 and among those with limited schooling.67 Studies conducted in Brazil confirm these findings.68-71 Therefore, in order to reduce smoking during pregnancy, more money should be invested, not only in health programs but also in education, with special priority given to adolescents.72

Even minimal interventions can produce success rates as high as 30% in the general population.73 The results of these efforts are even higher when specifically targeted towards pregnant women58,74. Gestation and the postpartum period offer extraordinary opportunities for the promotion of smoking cessation.75 In light of this, a portion of every prenatal appointment should be dedicated to the discussion of smoking and its consequences. This type of counseling should also be given to pregnant women who are passive smokers76 and to their smoking husbands, since the situation constitutes a predictive factor for smoking cessation program failure.67

In Brazil, nicotine dependence generates such a demand for smoking cessation services that there is a waiting list for enrollment.77 In order to attenuate this problem, the Brazilian Ministry of Health released a government directive in August of 2002,78 funding antismoking programs within the public health care system. However, specific programs targeting pregnant women have not yet been established.

Drug therapy and counseling have proven efficacious in promoting smoking cessation. Each has its own degree of efficacy, but, when used in combination, they increase overall success rates.79 The combination of counseling and the use of bupropion, with or without nicotine replacement therapy (NRT), produces an initial cessation rate from 40% to 60% and, after one year, from 25% to 30%.79 Drug therapy for smoking cessation is of limited use in pregnant women. Since the drugs may be toxic for the fetus, their use has an uncertain risk-benefit relationship. This reinforces the necessity for smoking cessation programs, even prior to conception.

Dempsey e Benowitz,7 in a detailed review article on the use of NRT during gestation, state that when pregnant women are not able to quit smoking with the aid of nonpharmacologic therapies alone, NRT should be considered. This type of adjunctive therapy doubles the cessation rate, increasing the chance of mother and fetus being spared from the more than 4700 toxic substances (other than nicotine), especially carbon monoxide, found in tobacco smoke. The authors consider carbon monoxide the most toxic substance in tobacco smoke. Intermittent-use formulations of NRT (nicotine gum, for example) are preferred during pregnancy because the total dose of nicotine delivered to the fetus will be less than with continuous-use formulations (transdermal patches). In addition, Dempsey and Benowitz recommend the use of NRT for mothers who need to quit smoking and are breastfeeding, since minimal amounts of nicotine are excreted into breast milk, with minimum risk for the baby compared to the beneficial protection against second-hand smoke. Other authors80,81 also state that, although the use of NRT is not ideally recommended during pregnancy, it is safer to use NRT than to continue smoking.

Due to the limitations of drug therapy for promoting smoking cessation during pregnancy, psychological aspects of smoking dependence must be approached through psychotherapy. Depending on the degree to which the pregnant woman is motivated, various techniques can be successfully used, individually or in groups.79,82-84 Motivational interviews can be used with those who are ambivalent, and cognitive behavior therapy can be used with those who are already motivated. Cognitive behavior therapy is the method of first choice for smoking cessation therapy57 and is also included in the program suggested by the Ministry of Health in Brazil.85 Counseling in person or over the phone have also proven efficacious.79,82 Self-help materials that provide practical counseling for smoking cessation summarized in booklets, cassettes, videocassettes and software have shown limited results when used in isolation, but can be useful when contextually combined with other forms of intervention.59 These more targeted (at a specific group) these auxiliary materials are, the more effective they are.79,82 Hence, it is important that public and private antismoking campaigns develop individualized programs and materials for pregnant women. Unlike Canada, England, and the USA, Brazil has not established a policy to promote smoking cessation during pregnancy. Online programs and recommendations42,86 providing practical information that is specifically targeted at pregnant women (www.surgeongeneral.gov/tobacco/prenatal.htm, www.cctc.ca and www.smokefreefamilies.uab.edu/bpi_form.htm), have shown excellent results and can be used as models for regional programs on the same scale in Brazil.

Prevention of smoking relapse

Smoking cessation at the beginning of gestation considerably reduces risks to fetal health.4 If the smoker remains abstinent throughout the postpartum period, newborns will not be exposed to the harmful substances found in tobacco smoke, which are associated with various diseases, especially respiratory infections. When abstinence is maintained, the quality of life improves for the child and the risk of smoking-related disease decreases for the mother. Therefore, concern about smoking relapse is justified.

Although from 25% to 40% of women quit smoking or drastically reduce their smoking when they become aware of their pregnancy,59,87,88,89 relapse during the prepartum or postpartum period is quite frequent. It is estimated that 12% to 15% of pregnant women who quit smoking (either spontaneously or with treatment) will relapse during pregnancy.90 The risk of postpartum relapse is even higher, increasing from 40% to 90% over the first 12 months after giving birth.91,92

The variables most frequently cited as predictive of smoking relapse during pregnancy are disbelief of data regarding the hazardous effects that smoking has on the fetus, lack of confidence in their own capacity for maintaining cessation, multipara status, lack of social support (living with smokers), stress, a short period of cessation prior to the first prenatal visit, limited schooling, and youth.88,93

Quinn et al.,93 in a study conducted in California, evaluated the behavior of pregnant women who spontaneously quit smoking during pregnancy and reported a relapse rate of approximately 21% in the prepartum period. Accordingly, they raised an alert regarding the high relapse rate among pregnant women who quit smoking spontaneously and recommended that they be identified and included in a special program for relapse prevention, rather than simply being praised, as is the normal practice.

On the other hand, Secker-Walker et al.94 showed that relapse prevention programs offered during the prenatal and postnatal periods to pregnant smokers who quit smoking (spontaneously or with treatment) do not affect the long-term relapse rate during the postpartum period. However, these programs do prolong the abstinence period, which justifies their being offered to all groups of pregnant women. Other studies also report the effectiveness of these programs, independently of the long-term relapse rate.91

In a prospective study, McBride et al.95 observed 106 women who had quit smoking during pregnancy. By the sixth postpartum week, 24% had resumed smoking with regularity and, by the end of the sixth postpartum month, the relapse rate had reached 40%. In accordance with the findings of Fingerhut96 and Mullen,92 McBride et al. observed that the risk for relapse increased gradually, being highest around the fourth postpartum month, differing from that seen in other groups of recent ex-smokers, which present early relapse (after only a few days or weeks).

Factors associated with the risk of postpartum relapse are smoking cessation late ,during pregnancy,96 early interruption of breastfeeding,97,98 weight gain,97 the stress of caring for an infant,99 cohabitation with a smoker95 and postpartum depression.60 Further risk is created when the maternal leave ends and the mother, in addition to housework, has to cope with professional issues and work alongside other female smokers.

Intensive effort should be made with the aim of prevention and treatment of relapse, since it may jeopardize the excellent chances of permanent smoking cessation presented by the motivational aspects of pregnancy.

Final comments

The hazardous effects of tobacco smoke affect not only pregnant women but also the fetus, which becomes a truly active smoker within the womb.

Recent data from the WHO reveals that, worldwide, approximately five million people per year die due to tobacco use.100 These alarming data underscore the need for antismoking campaigns.

Pregnant women should be the focus of interventions. Cessation programs targeting the general population show much less promising results than those specifically targeting pregnant women, in which the cost-benefit relationship is optimized. Through the elimination of maternal and fetal exposure to the effects of smoking and the protection of newborns, children, and other relatives from second-hand smoke, satisfactory results can be achieved with little investment. The influence that mothers have on their children is fundamental. The habits of the mother direct the social behavior of the child and may influence decisions about smoking made by future generations.

Special consideration should be given to certain subgroups among pregnant women, and specific strategies for optimizing the approach taken towards smoking during pregnancy should be planned accordingly. Since smoking cessation prior to conception assures maximum protection of the fetus and drug therapy for nicotine dependence can be used without restrictions prior to pregnancy, all fertile women of childbearing age should be targeted. Pregnant women with little schooling should also be a focus since smoking is higher within this group. In addition, pregnant women who spontaneously quit smoking should be targeted because of the high prevalence of relapse. Furthermore, antismoking campaigns should include provisions for educating smoking husbands because they influence smoking behavior in their pregnant wives. Since there is a high risk of relapse after gestation, and postpartum follow-up is essential to guaranteeing permanent cessation, women who quit smoking during pregnancy should also be targeted.

Obstetricians and pediatricians, as well as nurses and other health personnel, should be aware of antismoking strategies and should be trained in such. These professionals are at the core of the success of smoking cessation programs during pregnancy and early childhood. It is necessary to create a well-defined policy for smoking cessation during pregnancy if we want this to become a reality in our country. All segments of our society, such as the government, the press, jurists, educators, religious leaders and corporate councils, as well as health care groups and associations, should recognize the importance of such policies to improving of the quality of life in our country. Within this context, we must highlight the fact that prevention and reduction of smoking is the best and the least expensive method of preventing various diseases and minimizing the need for treatment of those diseases.

References

66 SAMHSA 1997. Office of Applied Studies, Substance Abuse and Mental Health Services Administration. Preliminary results from the 1996 national household survey on drug abuse. Rockville, MD: SAMHSA; 1997. p.90:Table 32B. DHHS Publication (SMA) 97-3149.

Submitted: 16 July 2003.

Accepted, after revision: 20 November 2003.

References

  • 1 from the Centers for Disease Control. Health benefits of smoking cessation. JAMA 1990;264:1930.
  • 2 Lambers DS, Clark KE. The maternal and fetal physiologic effects of nicotine. Semin Perinatol 1996;20:115-26.
  • 3 Medical-care expenditures attributable to cigarette smoking during pregnancy - United States, 1995. MMWR Morb Mortal Wkly Rep 1997;46:1048-50.
  • 4 Butler NR, Goldstein H, Ross EM. Cigarette smoking in pregnancy: its influence on birth weight and perinatal mortality. Br Med J 1972;2:127-30.
  • 5 Youth tobacco surveillance - United States, 1998-1999. MMWR CDC Surveill Summ 2000;49:1-94.
  • 6 Aligne CA, Stoddard JJ. Tobacco and children. An economic evaluation of the medical effects of parental smoking. Arch Pediatr Adolesc Med 1997;151:648-53.
  • 7 Dempsey DA, Benowitz NL. Risks and benefits of nicotine to aid smoking cessation in pregnancy. Drug Saf 2001;24:277-322.
  • 8 Cutler AR, Wilkerson AE, Gingras JL, Levin GD. Prenatal cocaine and/or nicotine exposure in rats: preliminary findings on long-term cognitive outcome and genital development at birth. Neurotoxicol Teratol 1996;18:635-643.
  • 9 Schlumpf M, Gahwiler M, Ribary U, Lichtensteiger W. A new device for monitoring early motor development: prenatal nicotine-induced changes. Pharmacol Biochem Behav 1988;30:199-203.
  • 10 Peters DA, Tang S. Sex-dependent biological changes following prenatal nicotine exposure in the rat. Pharmacol Biochem Behav 1982;17:1077-1082.
  • 11 Slotkin TA. Fetal nicotine or cocaine exposure: which one is worse? J Pharmacol Exp Ther 1998;285:931-45.
  • 12 Schoendorf KC, Kiely JL. Relationship of sudden infant death syndrome to maternal smoking during and after pregnancy. Pediatrics 1992;90:905-8.
  • 13 Slotkin TA, Lappi SE, McCook EC, Lorber BA, Seidler FJ. Loss of neonatal hypoxia tolerance after prenatal nicotine exposure: implications for sudden infant death syndrome. Brain Res Bull 1995;38:69-75.
  • 14 Gilliland FD, Berhane K, McConnell R, Gauderman WJ, Vora H, Rappaport EB, Avol E, Peters JM. Maternal smoking during pregnancy, environmental tobacco smoke exposure and childhood lung function. Thorax 2000;55:271-6.
  • 15 Gilliland FD, Li YF, Peters JM. Effects of maternal smoking during pregnancy and environmental tobacco smoke on asthma and wheezing in children. Am J Respir Crit Care Med 2001;163:429-36.
  • 16 Elliot JG, Carroll NG, James AL, Robinson PJ. Airway alveolar attachment points and exposure to cigarette smoke in utero. Am J Respir Crit Care Med 2003;167:45-9.
  • 17 Sherrill DL, Lebowitz MD, Knudson RJ, Burrows B. Smoking and symptom effects on the curves of lung function growth and decline. Am Rev Respir Dis 1991;144:17-22.
  • 18 Tager IB, Weiss ST, Munoz A, Rosner B, Speizer FE. Longitudinal study of the effects of maternal smoking on pulmonary function in children. N Engl J Med 1983;309:699-703.
  • 19 Newnham JP, Patterson L, James I, Reid SE. Effects of maternal cigarette smoking on ultrasonic measurements of fetal growth and on doppler flow velocity waveforms. Early Hum Dev 1990;24:23-36.
  • 20 Jarvis M, Tunstall-Pedoe H, Feyerabend C, Vesey C, Salloojee Y. Biochemical markers of smoke absorption and self-reported exposure to passive smoking. J Epidemiol Community Health 1984;38:335-9.
  • 21 Sauter D. Hematologig principles. In: Goldfrank LR, Weisman RS, Flomenbaum NE, et al., editors. Toxicologic emergencies. Norwalk: Appleton & Lange; 1994.
  • 22 Crowley TJ, Andrews AE, Cheney J, Zerbe G, Petty TL. Carbon monoxide assessment of smoking in chronic obstructive pulmonary disease. Addict Behav 1989;14:493-502.
  • 23 Longo LD. The biological effects of carbon monoxide on the pregnant woman, fetus, and newborn infant. Am J Obstet Gynecol 1977;129:69-103.
  • 24 Gabriel R, Alsat E, Evain-Brion D. Alteration of epidermal growth factor receptor in placental membranes of smokers: relationship with intrauterine growth retardation. Am J Obstet Gynecol 1994;170:1238-43.
  • 25 Buchan PC. Cigarette smoking in pregnancy and fetal hyperviscosity. Br Med J (Clin Res Ed) 1983;286:1315.
  • 26 Bureau MA, Shapcott D, Berthiaume Y, Monette J, Blouin D, Blanchard P, et al. Maternal cigarette smoking and fetal oxygen transport: a study of P50, 2,3-Diphosphoglycerate, total hemoglobin, hematocrit, and type f hemoglobin in fetal blood. Pediatrics 1983;72:22-6.
  • 27 Penney DG. Effects of carbon monoxide exposure on developing animals and humans. In: Penney DG, editor. Carbon monoxide. Boca Raton: CRC Press; 1996. p.109-44.
  • 28 Clubb FJ, Jr., Penney DG, Baylerian MS, Bishop SP. Cardiomegaly due to myocyte hyperplasia in perinatal rats exposed To 200 Ppm carbon monoxide. J Mol Cell Cardiol 1986;18:477-86.
  • 29 Schellenberg JC, North RA, Taylor R, Zhou RL. Secretory component of immunoglobulin A in maternal serum and the prediction of preterm delivery. Am J Obstet Gynecol 1998;178:535-9.
  • 30 Meyer MB, Tonascia JA. Maternal smoking, pregnancy complications, and perinatal mortality. Am J Obstet Gynecol 1977;128:494-502.
  • 31 Hadley CB, Main DM, Gabbe SG. Risk factors for preterm premature rupture of the fetal membranes. Am J Perinatol 1990;7:374-9.
  • 32 Barrett B, Gunter E, Jenkins J, Wang M. Ascorbic acid concentration in amniotic fluid in late pregnancy. Biol Neonate 1991;60:333-5.
  • 33 Anderson R. Effects of ascorbate on leucocytes: part II. Effects of ascorbic acid and calcium and sodium ascorbate on neutrophil phagocytosis and post-phagocytic metabolic activity. S Afr Med J 1979;56:401-4.
  • 34 Phillips CL, Tajima S, Pinnell SR. Ascobic acid and transforming growth factor-B-1 increase collagen biosynthesis via different mechanismis: coordinate regulation of pro-alpha-1(I) and pro-alpha-1(III) collagens. Arch Biochem Biophys 1982;295:397-403.
  • 35 Sastry BV. Placental toxicology: tobacco smoke, abused drugs, multiple chemical interactions, and placental function. Reprod Fertil Dev 1991;3:355-72.
  • 36 French JI, Mcgregor JA. The pathobiology of premature rupture of membranes. Semin Perinatol 1996;20:344-68.
  • 37 Keelan JA, Coleman M, Mitchell MD. The molecular mechanisms of term and preterm labor: recent progress and clinical implications. Clin Obstet Gynecol 1997;40:460-78.
  • 38 Klerman LV, Rooks JP. A simple, effective method that midwives can use to help pregnant women stop smoking. J Nurs Midwifery 1999;44:118-23.
  • 39 Murray RP, Connett JE, Lauger GG, Voelker HT. Error in smoking measures: effects of intervention on relations of cotinine and carbon monoxide to self-reported smoking. The Lung Health Study Research Group. Am J Public Health 1993;83:1251-7.
  • 40 Glasgow RE, Mullooly JP, Vogt TM. Biochemical validation of smoking status: pros, cons, and data from four low-Intensity interventio. Addict Behav 1993;18:511-27.
  • 41 Velicer WF, Prochaska JO, Rossi JS, Snow MG. Assessing outcome in smoking cessation studies. Psychol Bull 1992;111:23-41.
  • 42 Windsor RA, Woodby LL, Miller TM, Hardin JM, Crawford MA, DiClemente CC. Effectiveness of agency for health care policy and research clinical practice guideline and patient education methods for pregnant smokers in medicaid maternity care. Am J Obstet Gynecol 2000;182:68-75.
  • 43 Secker-Walker RH, Vacek PM, Flynn BS, Et Al. Exhaled carbon monoxide and urinary cotinine as measures of smoking In pregnancy. Addict Behav 1997;22:671-84.
  • 44 Laranjeira R, Pillon SC, Dunn J. Environmental tobacco smoke exposure among non-smoking waiters: measurement of expired carbon monoxide levels. Rev Paul Med 2000;118:89-92.
  • 45 Adams EK, Melvin CL. Costs of maternal conditions attributable to smoking during pregnancy. Am J Prev Med 1998;15:212-9.
  • 46 Ronald F, Cobun MD. Endogenous carbon monoxide production. N Engl J Med 1970;282:207-9.
  • 47 Halpern R, Schaefer ES, Pereira A da S, Arnt EM, Bezerra JP, Pinto dos S. Risk factors for low birth weight in a rural community in southern Brazil. J Pediatr 1996;72:369-73.
  • 48 WHO. Division of Family Planning. The incidence of low birth weight. A critical review of available information. World Health Stat Q 1980;33:197-224.
  • 49 Difranza JR, Lew RA. Effect of maternal cigarette smoking on pregnancy complications and sudden infant death Syndrome. J Fam Pract 1995;40:385-94.
  • 50 Marks JS, Koplan JP, Hogue CJ, Dalmant ME. A cost-benefit/cost-effectiveness analysis of smoking cessation for pregnant women. Am J Prev Med 1990;6:282-9.
  • 51 Adams EK, Miller VP, Ernst C, Nishimura BK, Melvin C, Merritt R. Neonatal health care costs related to smoking during pregnancy. Health Econ 2002;11:193-206.
  • 52 Difranza JR, Lew RA. Morbidity and mortality in children associated with the use of tobacco products by other people. Pediatrics 1996;97:560-8.
  • 53 Doubilet P, Weinstein MC, McNeil BJ. Use and misuse of the term "cost effective" in medicine. N Engl J Med 1986;314:253-6.
  • 54 Ravenholt RT. Tobacco's impact on twentieth-century u.s. mortality patterns. Am J Prev Med 1985;1:4-17.
  • 55 The World Bank. Curbing the epidemic: governments and the economics of tobacco control. Washington: The World Bank; 1999. Series: Development in practice.
  • 56 Secker-Walker RH, Vacek PM, Flynn BS, Mead PB. Estimated gains in birth weight associated with reductions in smoking during pregnancy. J Reprod Med 1998;43:967-74.
  • 57 Rigotti NA. Clinical practice. Treatment of tobacco use and dependence. N Engl J Med 2002;346:506-12.
  • 58 Melvin CL, Dolan-Mullen P, Windsor RA, Whiteside HP Jr, Goldenberg RL. Recommended cessation counselling for pregnant women who smoke: a review of the evidence. Tob Control 2000;9(Suppl 3):III80-84.
  • 59 Windsor RA, Lowe JB, Perkins LL, Smith-Yoder D, Artz L, Crawford M, et al. Health education for pregnant smokers: its behavioral impact and cost benefit. Am J Public Health 1993;83:201-6.
  • 60 Orleans CT, Barker DC, Kaufman NJ, Marx JF. Helping pregnant smokers quit: meeting the challenge in the next Decade. Tob Control 2000;9(Suppl 3):III6-11.
  • 61 Connor SK, Mcintyre L. The sociodemographic predictors of smoking cessation among pregnant women in Canada. Can J Public Health 1999;90:352-5.
  • 62 US Dept of Health and Human Services. Healthy people 2000 review. Washington, DC: Office of Disease Prevention and Health Promotion; 1998-1999. DHHS Publication (PHS) 99-1256.
  • 63 Pickett KE, Abrams B, Schauffler HH, Savage J, Brandt P, Kalkbrenner A, et al. Coverage of tobacco dependence treatments for pregnant smokers in health maintenance organizations. Am J Public Health 2001;91:1393-4.
  • 64 Mcphillips-Tangum C. Results from the first annual survey on addressing tobacco in managed care. Tob Control 1998;7(Suppl):S11-13.
  • 65 Raw M, Mcneill A, West R. Smoking cessation guidelines for health professionals. A guide to effective smoking cessation interventions for the health care system. Health education authority. Thorax 1998;53(Suppl 5 Pt 1):S1-19.
  • 67 Ebrahim SH, Floyd RL, Merritt RK 2nd, Decoufle P, Holtzman D. Trends in pregnancy-related smoking rates in the United States, 1987-1996. JAMA 2000;283:361-6.
  • 68 Horta BL, Victora CG, Barros FC, dos Santos I da S, Menezes AM. Tobacco smoking among pregnant women in an urban area in southern Brazil, 1982-93. Rev Saude Publica 1997;31:247-53.
  • 69 Gross R, Mauad Filho F, Netto AR, Sobrinho FM, Ferreira DL, Mucallo G, et al. Smoking and pregnancy. I. Prevalence of the smoking habit among pregnant women. Rev Assoc Med Bras 1983;29:4-6.
  • 70 Simoes MJ. Study of yhe frequency of mothers' smoking habits during pregnancy in Ribeirão Preto - SP. Rev Cienc Biomed 1985;6:61-9.
  • 71 Halal IS, Victoria CG, Barros FC. Determining factors related to smoking and its abandonment during pregnancy in an Urban locality in southern Brazil. Rev Saude Publica 1993;27:105-12.
  • 72 Albrecht S, Cassidy B, Reynolds MD, Ketchem S, Abriola D. Developing guidelines for smoking cessation interventions for pregnant adolescents. J Pediatr Nurs 1999;14:150-6.
  • 73 Fiore MC. The new vital sign. assessing and documenting smoking status. JAMA 1991;266:3183-4.
  • 74 Laml T, Hartmann BW, Kirchengast S, Preyer O, Albrecht AE, Husslein PW. Impact of maternal anthropometry and smoking on neonatal birth weight. Gynecol Obstet Invest 2000;50:231-6.
  • 75 Diclemente CC, Dolan-Mullen P, Windsor RA. The process of pregnancy smoking cessation: implications for interventions. Tob Control 2000;9(Suppl 3):III16-21.
  • 76 Wenderlein JM. Smoking and pregnancy. Z Arztl Fortbild (Jena) 1995;89:467-71.
  • 77 Malbergier A. Tabagismo. J Bras Dep Quim 2001;2:47-51.
  • 78 Brasil. Ministério da Saúde. Programa Nacional de Controle do Tabagismo. Fumo. Portaria 1575/GM do MS. DOU 170, 03 set. 2002.
  • 79 Fiore MC, Bailey WC, Cohen SJ, et al. Treating tobacco use and dependence. Rockville, MD: Department of Health and Human Services, Public Health Service; 2000.
  • 80 Gigliotti A, Laranjeira R. Terapêutica do tabagismo. J Bras Med 1999;77:66-78.
  • 81 WHO. Women and the tobacco epidemic: challenges for the 21st century. Geneva; 2001.
  • 82 Lancaster T, Stead L, Silagy C, Sowden A. Effectiveness of interventions to help people stop smoking: findings from the Cochrane Library. BMJ 2000;321:355-8.
  • 83 Miller WR, Rollnick S. Miller WR, Rollnick S. Motivational interviewing: preparing people for change. New York: Guiford Press; 1991.
  • 84 Leite JC, Franken RA. Group psychotherapy in the treatment of nicotine dependence: the experience at Santa Casa of São Paulo. Rev Soc Cardiol Estado São Paulo 1999;6(Suppl A):1-10.
  • 85 INCA - Instituto Nacional do Câncer. Abordagem e tratamento do fumante - consenso 2001. Rio de Janeiro: INCA; 2001.
  • 86 Walsh RA, Redman S, Brinsmead MW, Byrne JM, Melmeth A. A smoking cessation program at a public antenatal clinic. Am J Public Health 1997;87:1201-4.
  • 87 Ershoff DH, Mullen PD, Quinn VP. A randomized trial of a serialized self-help smoking cessation program for pregnant women in an HMO. Am J Public Health 1989;79:182-7.
  • 88 Valbo A, Schioldborg P. Smoking in pregnancy: a follow-up study of women unwilling to quit. Addict Behav 1993;18:253-7.
  • 89 Floyd RL, Rimer BK, Giovino GA, Mullen PD, Sullivan SE. A review of smoking in pregnancy: effects on pregnancy outcomes and cessation efforts. Annu Rev Public Health 1993;14:379-411.
  • 90 Petersen L, Handel J, Kotch J, Podedwomy T, Rosen A. Smoking reduction during pregnancy by a program of self-help and clinical support. Obstet Gynecol 1992;79:924-30.
  • 91 Mcbride CM, Curry SJ, Lando HA, Pirie PL, Grothaus LC, Nelson JC. Prevention of relapse in women who quit smoking during pregnancy. Am J Public Health 1999;89:706-11.
  • 92 Mullen PD, Quinn VP, Ershoff DH. Maintenance of nonsmoking postpartum by women who stopped smoking during pregnancy. Am J Public Health 1990;80:992-4.
  • 93 Quinn VP, Mullen PD, Ershoff DH. Women who stop smoking spontaneously prior to prenatal care and predictors of relapse before delivery. Addict Behav 1991;16:29-40.
  • 94 Secker-Walker RH, Solomon LJ, Flynn BS, Skelly JM, Lepage SS, Goodwin GD, et al. Smoking relapse prevention counseling during prenatal and early postnatal care. Am J Prev Med 1995;11:86-93.
  • 95 Mcbride CM, Pirie PL, Curry SJ. Postpartum relapse to smoking: a prospective study. Health Educ Res 1992;7:381-90.
  • 96 Fingerhut LA, Kleinman JC, Kendrick JS. Smoking before, during, and after pregnancy. Am J Public Health 1990;80:541-44.
  • 97 Mcbride CM, Pirie PL. Postpartum smoking relapse. Addict Behav 1990;15:165-68.
  • 98 O'Campo P, Faden RR, Brown H, Gielen AC. The impact of pregnancy on women's prenatal and postpartum smoking behavior. Am J Prev Med 1992;8:8-13.
  • 99 Edwards N, Sims-Jones N. Smoking and smoking relapse during pregnancy and postpartum: results of a qualitative study. Birth 1998;25:94-100.
  • 100 WHO. The tobacco atlas. Geneva; 2002.
  • Correspondence
    Waldir Leopércio
    Rua Conde de Irajá, 420
    Rio de Janeiro, Brasil Cep: 22271-020
    Phone/fax: (21) 2535-5910
    e-mail: cdtorax@terra.com.br
  • *
    Study carried out at the Instituto de Doenças do Tórax da Universidade Federal do Rio de Janeiro.
  • Publication Dates

    • Publication in this collection
      08 June 2004
    • Date of issue
      Apr 2004

    History

    • Accepted
      20 Nov 2003
    • Received
      16 June 2002
    location_on
    Sociedade Brasileira de Pneumologia e Tisiologia SCS Quadra 1, Bl. K salas 203/204, 70398-900 - Brasília - DF - Brasil, Fone/Fax: 0800 61 6218 ramal 211, (55 61)3245-1030/6218 ramal 211 - São Paulo - SP - Brazil
    E-mail: jbp@sbpt.org.br
    rss_feed Acompanhe os números deste periódico no seu leitor de RSS
    Acessibilidade / Reportar erro