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Smoking and pregnancy outcome of adolescents
JOURNAL OF ADOLESCENT HEALTH CARE 2:115-120(1981)
Smoking and Pregnancy Outcome of Adolescents BETTY RUTH CARRUTH, Ph.D.
The interrelationship between dietary intake, smoking behavior, and weight gain during pregnancy was studied and compared with pregnancy outcomes of infant birth weight and Apgar scores of infants born to smokers. Nonsmokers (N = 28) and smokers (N = 39) were volunteers attending secondary schools in an urban area. Both groups received prenatal and tertiary care at free or reduced fees and participated in free lunch and other assistance programs at their schools. Smoking was not statistically related to maternal weight gain, infant birth weight, dietary inadequacy, or Apgar scores. Smoking was significantly related to low pregravid weight (P -< .05). Dietary iron and folic acid were deficient in both groups. Snacking represented a major source of calories, and 25-50% of foods consumed were eaten away from home. KEY WORDS:
Infant birth weight Nutrition Pregnancy Smoking The amount and frequency of smoking among teenage girls is increasing, particularly at the junior high age level (1). Smoking represents a health risk for the mother and fetus. Rush reports a negative relationship between frequency of smoking and the overall calorie intake of pregnant adolescents (2). During pregnancy there is an increased need for nutrients and calories to provide adequate maternal weight gain and nutrient tissue saturation. Smoking
has been associated with increased perinatal death and neonatal morbidity of infants born to adolescents. The relationship between the frequency of smoking and infant birth weight is well documented (3). On the average, infants born to smokers weigh 150-250 g less than the infants of nonsmokers. The frequency of live infants born to smokers that weigh less than 2500 g was approximately twice that of infants born to nonsmokers. Davies et al. reported that heavy smokers, i.e., 15 cigarettes or more per day, had infants with smaller head circumference and shorter recumbent heights than infants born to nonsmokers (4). In a retrospective review of records of 18,919 normal term singleton births, Garnet al. concluded that smoking during pregnancy was the most preventable factor in reducing the incidence of low-birthweight infants (5). The mechanism by which smoking reduces birth weight involves two hypotheses: (1) smoking decreases food intake, thus reducing maternal weight gain and indirectly reducing birth weight; and (2) fetal hypoxia occurs as a result of uteroplacental vasoconstriction in the presence of elevated blood levels of nicotinic acid (6). Fetal hypoxia is supported by Ausmussen's study of the ultrastructure of placental villi in heavy smokers (-> 10 cigarettes/day). There are fewer fetal capillaries, thickening of the basement membrane of the placenta as well as larger amounts of filaments and fibrillae, which may decrease placental blood flow
(7). From the Adolescent Health Training Project, Department of Pediatrics, Southwestern Medical School, 5323 Harry Hines Boulevard, Dallas, Texas. Direct reprint requests to: Betty Ruth Carruth, Ph.D., Director of Nutrition, Adolescent Health Training Project, Department of Pediatrics, Southwestern Medical School, 5323 Harry Hines Blvd., Dallas, TX 75235. Manuscript accepted May 16, 1981.
The decrease in food intake of smokers occurs in both humans and animals, although the mechanism is not clearly understood. Infants born to smokers reportedly have a lower birth weight than infants of nonsmokers. Food and nutrient intake during pregnancy is especially important in adolescent girls, because of the interrelationship of adequate calorie
© Society for Adolescent Medicine, 1981 Published by Elsevier North Holland, Inc., 52 Vanderbflt Ave., New York, NY 10017
115 0197-0070/81/020115 + 6 $02.75
116
CARRUTH
intake, maternal weight gain, and infant birth weight. Nutrient and caloric requirements during pregnancy are increased over those of nonpregnant teenagers. Based on the Recommended Dietary Allowances (RDAs), the mean calorie allowance is 2200 kcal/day for ages 11-14 and 2100 kcal/day for older, nonpregnant adolescents (8). With the addition of 300 kcal/day during pregnancy, energy allowances should be 2500 kcal/day for the younger age group and 2400 kcal/day for ages 15-18 years. Some have recommended even higher energy levels by adding an additional 200 kcal/day or more to ensure a positive energy balance (9). Recent surveys of females in the United States showed an average calorie intake for girls ages 12-14 of 1900 kcal/day, and for ages 15-17, 1750 kcal/day, respectively (10). Reported dietary deficiencies for female adolescents include calcium, iron, vitamin A, folacin, riboflavin, and pyridoxine (11-13). Daniel et al. found that 90% of girls from low-income families and all girls from upper-income families consumed less than 50% of the RDAs of folacin for nonpregnant females. A better socioeconomic status did not predict better dietary intakes of iron and folate-rich foods (13). In general, the literature concerning smoking and low birth weight indicates a negative association between these factors and that food intake is decreased by smoking behavior. However, Hollingsworth et al. did not find this relationship among teenagers classified as light smokers (14). One could postulate that food intake was depressed in heavy smokers prior to pregnancy and that food consumption was not increased significantly during gestation. If the average intake is 1700-1900 kcal/day and the recommended allowances for pregnancy range from 2400 to 2700 kcal/day, then many girls must add 700-1000 kcal/day to their normal consumption patterns to meet pregnancy requirements. This study compares the dietary habits and smoking behavior of pregnant adolescents and relates these to infant birth weight and Apgar score.
Methods Sample Selection Sixty-seven pregnant volunteers were recruited from secondary schools in a northern urban city with a primarily white population (95%). Twenty-eight nonsmoking pregnant adolescents attended a special education program apart from the mainstream
JOURNAL OF ADOLESCENT HEALTH CARE Vol. 2, No. 2
population. The curriculum and services were part of the public education system. Thirty-nine pregnant smokers were enrolled from a regular public school mainstream program. Both groups received their prenatal and free and/ or reduced services at community clinics and the tertiary hospitals providing acute medical care. In addition, most participants used the free and/or reduced school lunch programs and received food stamps and other types of assistance from the community. Initial contact was made through school and clinic nurses, physicians, and brief presentations to student groups. Interested girls were then personally contacted, and the purpose of the study was explained verbally and in writing. Consent forms were signed by the teenager and the responsible adult in the family prior to entry into the study. No incentives were given for participation and no effort was made to follow up those who chose not to participate. The research protocol met the standards established by the appropriate university committee for h u m a n research. Cooperating schools, physicians, clinics, and if required, administrators of medical records provided letters of agreement.
Data Collection The initial prenatal visit for the smokers included a history and physician examination, urinalysis, hemogram, rubella titer RH and antibody levels, pap smear, and GC culture. Skinfold measurements, taken with a Lange caliper, at tricep and subscapular sites followed the National Research Council Committee on Nutritional Anthropometry procedures (15). Heights and weights were taken on a beam scale and rod and recorded in centimeters and kilograms. Skinfold measurements were not done on the nonsmoker group. For both groups, a trained nutritionist conducted the initial dietary interview, employing a standard format for asking about and recording food intake for the previous 24 hours and probing for usual food intake. Estimates of amounts eaten were compared with standardized food models. In evaluating group data, 24-hour recalls with 50 or more responses were considered adequate (16). Alcohol, tobacco, and food consumption patterns away from home were assessed by history. For the smoker group, dietary interviews and anthropometric measurements were repeated in the
December 1981
SMOKING AND PREGNANCY OUTCOME
117
Table 1. Comparison of Pregnant Adolescents: Nonsmokers vs. Smokers Onset of menses (yr)
Time between menses and conception (yr)
Location
Height (cm)
Pregravld weight (kg)
Nonsmokers (N = 28)
158.1 +_ 5.8
52.7 _+ 5.9*
12.5 + 1.1
4.0 _+ 1.6
Smokers (N = 39)
163.5 _+ 5.7
56.3 +- 8.4*
12 6 + 1.4
4.3 _+ 1 5
*P -< 0.05, mean _+ S.D.
last trimester. The sequencing of appointments and laboratory analyses throughout gestation followed protocols set up by the clinic physicians. Iron and folacin supplements were given at the initial visit, irrespective of hematologic: values. A history of chronic disease and/or previously identified obstetric problems precluded participation in the study. Infant birthweights and Apgar scores were recorded at the time of delivery and weight data were collected over a period of one to three months. Medical records and physician's files provided the most detailed information. Gestational age is not reported, since it was frequently not given in weeks and inconsistently noted in records assessible to the researchers.
Data Analyses Chi square analysis and t-test were applied to determine statistical significance for group data. Measures of central tendency were computed for nutrient and anthropometric data. Dietary data were analyzed for calories, protein, calcium, iron, ascorbic acid, vitamin A, thiamin, riboflavin, and niacin. Agriculture Handbook No. 456 provided the nutrient data base for a computerized
analysis of food records (17). Manufacturers' product information, food labels, and published estimates for nutrient density by individual researchers provided information not in the handbook (18).
Results Table 1 describes the mean values for pregravid weight and height, age at onset of menses, and the time between menses and conception. With the exception of pregravid weight, there was no statistically significant difference between the two groups. The mean chronologic age for both groups was 16.3, with a range of 13-18 years. Range for age of onset of menses was 9-16 years. Onset of menarche for both groups occurred at a mean age close to the 12.3 years published by McGanity et al (19). Both groups met the criteria for gynecologic maturity, with 4.0 years or more between menarche and conception, hence a reproductive capacity similar to that of chronologically older w o m e n (9). For purposes of this research, gynecologic age rather than chronologic age was considered the primary variable. As shown in Table 2, nonsmokers consumed more calories than light smokers but less than heavy smokers (-> 15 cigarettes/day). Protein intake ex-
T a b l e 2. M e a n Calorie I n t a k e a n d N u t r i e n t A d e q u a c y for S m o k e r s vs. N o n s m o k e r s
Item~ Calories Protein (g) Calcium (mg) Iron (mg) Vitamin A (IU) Thiamin (mg) Riboflavin (mg) Niacin (mg) Vitamin C (mg) Folic acid (/~g)
Nonsmokers (N = 28) 2146.9 89.4 1125.6 13.3 7588.5 1.3 2.1 16.1 44.8 168.0
% RDAs
Less than 15 cigarettes/day (N = 21)
88.9 114.9 93.8 74.0 151.8 96.4 130.0 100.4 158.1 21.0
1944.6 85.5 1356.1 10.1 5705.4 1.2 23 13.2 139.6 302.7
~Food and Nutrition Board: Recommended Dmtary Allowances, 8 ed., 1974.
% RDAs
More than 15 cigarettes/day (N = 18)
% RDAs
81.0 115.6 113.0 56.1 114.1 85.0 137.4 82 8 232.6 37.8
2419.8 104.5 1903.1 12.5 8050.0 1.5 3.3 17.5 173.2 249.3
99.1 126.5 158.6 69~6 161 0 106.9 195.1 107.6 288.6 36.2
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CARRUTH
JOURNAL OF ADOLESCENT HEALTH CARE Vol. 2, No 2
ceeded 100% of the RDAs for pregnancy and, interestingly, the heavy smokers had the highest calcium consumption. Dietary iron was two-thirds or less of the reco m m e n d e d amount for nonpregnant adolescents and much less than the 30-60 mg of elemental iron frequently prescribed. Since it is estimated that the average American diet contains about 6 mg of iron per 1000 kcal, smokers and nonsmokers had similar calorie/iron ratios based on total daily caloric intake. Dietary folacin was less than 40% of the recommended allowance for pregnancy. Although food composition tables for folacin may be subject to criticism as a reference source, the girls did not choose foods that are considered rich sources of folacin. Choices of snacking foods tended to be high in protein and low in iron and folacin. All groups exceeded allowances for vitamins A, C, and riboflavin, whereas those smoking less than 15 cigarettes per day had lower intakes of thiamin and niacin than the nonsmokers and heavy smokers. A major source of high-quality protein, calcium, and riboflavin came from free milk served at breakfast, lunch, and as an after school snack. In general, participants limited consumption of cereal products and potatoes based on a belief that those particular foods were "fattening." From 25 to 50% of calories came from foods consumed away from home and at times other than the more conventional three meals per day food pattern. Table 3 depicts the mean birth weight and maternal weight gain for smokers and nonsmokers. The N = 23 represents the girls w h o reportedly maintained their smoking behavior during pregnancy and therefore should have an infant of lower birth weight. The infants of smokers were smaller, but both groups had normal weight infants. There was no significant difference between mean birth weights of infants born to light smokers (< 15 cigarettes) and those born to heavy smokers. In terms of parity, 79.5% were first births; 15.4%, second; and 5.1%, third. Apgar scores were within normal ranges for both groups.
One case of acetonuria (1 + ) occurred in a 16-yearold subject w h o had a history of drug abuse. Her infant weighed 2580 g, the lowest birth weight recorded. Naeye reported that fetuses of mothers 10-16 years of age grew more slowly, and acetonuria was considered a marker for high perinatal mortality in undernourished gestations (20). At the initial interview, tricep and subscapular fatfolds measured 17.6 and 14.2~mm, respectively. These values are almost identical to the fatfold measurements of 51 pregnant adolescents published by Morse et al. (21). The calculated mean arm fat area fell between the 50th and 85th percentile of values published for subjects measured in the Ten State Nutrition Survey for a comparable age distribution and race. These results indicate that at the initial interview, the smoker group had mean energy stores comparable with those reported for nonpregnant adolescents.
Discussion Our results do not support the concept that smoking influences food intake, thus adversely affecting infant birth weight. The discrepancy between our results and those reported in the literature may be related to a number of factors. First, our subjects' weight gain exceeded the current standards of 25-30 lbs (22). Second, in terms of gynecologic maturity, our group was more than 4 years post menarche at conception and could be expected to perform as more mature women. Third, the social and medical support services available to both groups increased the probability that problems could be identified earlier in the smokers' group. Fourth, because of the mean birth weights of babies born to our subjects, it is unlikely that the gestational ages were shortened compared with those of older women. Perhaps smoking merely identifies the girl who is socially advanced and reacts at an early age to perceived sociental norms as compared with her
T a b l e 3. P r e g n a n c y O u t c o m e for S m o k e r s vs. N o n s m o k e r s Mean Apgar scores
Group
Infant mean birth weight (g)
Mean maternal weight gain (kg)
1 min
5 rain
Nonsmokers
3280 + 482
14.1 +- 4.8
7.0
8.5
3225 + 336
14.8 + 4.0
8.8
9.0
(N = 28) Smokers (N = 23)
December 1981
peers (23). Yerushalmy observed that w o m e n w h o become smokers t e n d e d to have low-birth-weight infants before a n d after they begin to smoke. It was suggested that the greater incidence of low-birthweight infants m a y have been due to the patient a n d not to the smoking (24). Finally, the self-selection process in a voluntary s t u d y likely reflects some intrinsic motivation and personality characteristics that m a y contribute to our positive findings of better maternal a n d fetal health. Also, the exclusion of subjects with identified obstetric problems ensures a better outcome for group comparisons a n d m a y in some w a y exclude those w h o were more malnourished. The results of the s t u d y raise a major problem about attempting to relate p r e g n a n c y outcome to a single factor, since such factors as nutrition, prenatal care, a n d maternal weight gain are all interrelated. For example, the reported calorie intake of nonpregnant adolescents in tile United States ranges from about 1750 to 1950 cal/day. For the nonsmokers and light smokers, calorie estimates were 2100 and 1900 kcal/day, respectively, m u c h lower t h a n the 2400-2700 kcal/day r e c o m m e n d e d by various professional groups (9). However, other measures such as maternal weight gain and infant birthweight were within or exceeded r e c o m m e n d e d ranges. This creates a discrepancy that is not totally explained by the vagaries of dietary data or inaccuracies associated with recording medica]Ylaboratory data. H y t t e n suggests that potential adaptation systems within the maternal melieu m a y overcome a certain a m o u n t of the nutritional a n d environmental factors (25). However, this postulation does not hold true w h e n there are d o c u m e n t e d social a n d economic factors, such as food deprivation and inadequate prenatal care, that can result in infant and maternal morbidity. Our results clearly suggest that adolescents m a y have p r e g n a n c y outcomes similar to those of chronologically older w o m e n w h e n educational, health, and nutritional support systems are available to offset the potential influence of the subject's smoking during pregnancy. Our results also demonstrate h o w important snacking patterns of adolescents can be in attaining adequate nutrition. The reported energy intake was below the r e c o m m e n d e d allowances with snacking. Thus, omitting snacks would have resulted in major deficiencies for both smokers a n d nonsmokers. Consequently, the a u t h o r believes that dietary counselors should emphasize the positive aspects of snacking to pregnant adolescents and assist t h e m in making better food choices~
SMOKING AND PREGNANCY OUTCOME
119
Conclusion In a s t u d y of 67 p r e g n a n t adolescents, smoking was not significantly correlated with maternal weight gain, infant birth weight, or dietary inadequacy. Pregravid weight was significantly related to low infant birth weight at the P --- 0.05 level. Smoking status was not predictive of infant birth weight or Apgar scores. Both smokers a n d n o n s m o k e r s had major dietary deficiencies of iron and folacin and t e n d e d to c o n s u m e 25-50% of their food a w a y from h o m e or in small meals rather t h a n as part of a conventional eating pattern. An adequate diet, prenatal care, a n d maternal weight gain appeared to overcome the risk of smoking for this group. The data also suggest that girls are unlikely to meet dietary allowances for iron a n d folacin t h r o u g h food consumption and that snacking is an important source of calories a n d some nutrients. Acknowledgments Grateful acknowledgment is made to Shelley Kirk, Research Assistant, and Janet Machelett, student assistant, in gathering data.
Refet'ences 1. American Cancer Society:Summary of findings from a study about cigarette smoking among teenage girls and young women. Yankelovich, Skelly and White, Inc., 1976 2. Rush D: Examination of the relationship between birth weight, cigarette smoking during pregnancy and maternal weight gain. J Obstet Gynaecol Br Commonw 81:746-752, 1974 3. Abel EL: Smoking during pregnancy: A review of effects on growth and development of offspring. Hum Bio152:593-625, 1980 4. Davies DP, Gray OP, Ellwood PC et al: Cigarette smoking in pregnancy: Associations with maternal weight gain and fetal growth. Lancet 1 (7956): 385-387, 1976 5. Garn SM, Shaw HA, McCabe KD: Relativeeffects of smoking and other variables on size of newborn. Lancet 2 (8039): 667, 1977 6. Manning FA, Feyerabend C: Cigarette smoking and fetal breathing movements. Br J Obstet Gynaeco183:262-270, 1976 7. Asmussen h Ultrastructure of the villi and fetal capillaries in placentas from smoking and non-smoking mothers. Br J Obstet Gynaecol 87:239-245, 1980 8. Food and Nutrition Board: Recommended Dietary Allowances, 9th rev. ed., 1980. National Academy of Science, 1980 9. Task Force on Adolescent Pregnancy of The American College of Obstetricians and Gynecologists.Adolescent Perinatal Health, 1979 10. Vital and Health Statistics. Dietary Intake Findings, United States, 1971-1974. Series 11, No. 202. U.S. Govt. Prtg. Office, Washington, D.C., 1977. (Pub. No. (HRA) 77-1647) 11. Food Consumption Profilesof White and BlackPersons Aged 1-74 Years. United States, 1971-74. U.S. Govt. Prtg. Office, Washington, D.C., 1979. (DHEWPub. No. (PHS) 79-1658)
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12. Ten State Nutrition Survey, 1968-1970: Parts III and IV. (DHEW Pub. No. (HSM) 72-8131, 1972) 13. Daniel WA, Gaines EG, Bennett DL: Dietary retakes and plasma concentrations of folate in healthy adolescents. Am J Clin Nutr 28:363-370, 1975 14. Hollingsworth DR, Moser RJ, Carlson JW, et al: Abnormal adolescent primiparous pregnancy: Association of race, human chorionic somatomammotropin production, and smoking. Am J Obstet Gynecol 126:230-237, 1976 15. National Research Council Committee on Nutritional Anthropometry: Body measurement and human nutrition. Detroit, Wayne University Press, 1956 16. Chalmers FW, Clayton MM, Gates LO, et al: The dietary record--How many and which days? J Am Diet Assoc 28:711-717, 1952 17. United States Department of Agriculture--Agricultural Research Service: Nutritive Value of American Foods in Common Units, Agriculture Handbook No. 456, Washington, D.C., 1975 18. Perloff BP, Butrum RR: Folacin in selected foods. J Am Diet Assoc 70:161-172, 1977
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19. McGanity WJ, Little HM, Fogelman A, et ah Pregnancy in the adolescent. I. Preliminary summary of health status. Am J Obst Gynecol 103:773-788, 1969 20. Naeye RL: Teenaged and pre-teenaged pregnancies: Consequences of the fetal-maternal competition for nutrients. Pediatrics 67:146-150, 1981 21. Morse EH, Clarke RP, Merrow SG, et al: Comparison of nutritional status of pregnant adolescents with adult pregnant women. II. Anthropometric and dietary findings. Am J Clin Nutr 28:1422-1428, 1975 22. Worthington BS: Nutrition during pregnancy, lactation and oral contraception. Nurs Clin North Am 14:269-283, 1979 23. McKinney JP, Fitzgerald HE, Strommen EA: Developmental Psychology. The Adolescent and the Young Adult. Homewood, Illinois, The Dorsey Press, 1977 24. Yerushalmy J: Infants with low birthweight born before their mothers started to smoke cigarettes. Am J Obstet Gynecol 112:277-284, 1972 25. Hytten FE: Nutrition in pregnancy. Postgrad Med J 55:295-302, 1979
Smoking and Pregnancy Outcome of Adolescents BETTY RUTH CARRUTH, Ph.D.
The interrelationship between dietary intake, smoking behavior, and weight gain during pregnancy was studied and compared with pregnancy outcomes of infant birth weight and Apgar scores of infants born to smokers. Nonsmokers (N = 28) and smokers (N = 39) were volunteers attending secondary schools in an urban area. Both groups received prenatal and tertiary care at free or reduced fees and participated in free lunch and other assistance programs at their schools. Smoking was not statistically related to maternal weight gain, infant birth weight, dietary inadequacy, or Apgar scores. Smoking was significantly related to low pregravid weight (P -< .05). Dietary iron and folic acid were deficient in both groups. Snacking represented a major source of calories, and 25-50% of foods consumed were eaten away from home. KEY WORDS:
Infant birth weight Nutrition Pregnancy Smoking The amount and frequency of smoking among teenage girls is increasing, particularly at the junior high age level (1). Smoking represents a health risk for the mother and fetus. Rush reports a negative relationship between frequency of smoking and the overall calorie intake of pregnant adolescents (2). During pregnancy there is an increased need for nutrients and calories to provide adequate maternal weight gain and nutrient tissue saturation. Smoking
has been associated with increased perinatal death and neonatal morbidity of infants born to adolescents. The relationship between the frequency of smoking and infant birth weight is well documented (3). On the average, infants born to smokers weigh 150-250 g less than the infants of nonsmokers. The frequency of live infants born to smokers that weigh less than 2500 g was approximately twice that of infants born to nonsmokers. Davies et al. reported that heavy smokers, i.e., 15 cigarettes or more per day, had infants with smaller head circumference and shorter recumbent heights than infants born to nonsmokers (4). In a retrospective review of records of 18,919 normal term singleton births, Garnet al. concluded that smoking during pregnancy was the most preventable factor in reducing the incidence of low-birthweight infants (5). The mechanism by which smoking reduces birth weight involves two hypotheses: (1) smoking decreases food intake, thus reducing maternal weight gain and indirectly reducing birth weight; and (2) fetal hypoxia occurs as a result of uteroplacental vasoconstriction in the presence of elevated blood levels of nicotinic acid (6). Fetal hypoxia is supported by Ausmussen's study of the ultrastructure of placental villi in heavy smokers (-> 10 cigarettes/day). There are fewer fetal capillaries, thickening of the basement membrane of the placenta as well as larger amounts of filaments and fibrillae, which may decrease placental blood flow
(7). From the Adolescent Health Training Project, Department of Pediatrics, Southwestern Medical School, 5323 Harry Hines Boulevard, Dallas, Texas. Direct reprint requests to: Betty Ruth Carruth, Ph.D., Director of Nutrition, Adolescent Health Training Project, Department of Pediatrics, Southwestern Medical School, 5323 Harry Hines Blvd., Dallas, TX 75235. Manuscript accepted May 16, 1981.
The decrease in food intake of smokers occurs in both humans and animals, although the mechanism is not clearly understood. Infants born to smokers reportedly have a lower birth weight than infants of nonsmokers. Food and nutrient intake during pregnancy is especially important in adolescent girls, because of the interrelationship of adequate calorie
© Society for Adolescent Medicine, 1981 Published by Elsevier North Holland, Inc., 52 Vanderbflt Ave., New York, NY 10017
115 0197-0070/81/020115 + 6 $02.75
116
CARRUTH
intake, maternal weight gain, and infant birth weight. Nutrient and caloric requirements during pregnancy are increased over those of nonpregnant teenagers. Based on the Recommended Dietary Allowances (RDAs), the mean calorie allowance is 2200 kcal/day for ages 11-14 and 2100 kcal/day for older, nonpregnant adolescents (8). With the addition of 300 kcal/day during pregnancy, energy allowances should be 2500 kcal/day for the younger age group and 2400 kcal/day for ages 15-18 years. Some have recommended even higher energy levels by adding an additional 200 kcal/day or more to ensure a positive energy balance (9). Recent surveys of females in the United States showed an average calorie intake for girls ages 12-14 of 1900 kcal/day, and for ages 15-17, 1750 kcal/day, respectively (10). Reported dietary deficiencies for female adolescents include calcium, iron, vitamin A, folacin, riboflavin, and pyridoxine (11-13). Daniel et al. found that 90% of girls from low-income families and all girls from upper-income families consumed less than 50% of the RDAs of folacin for nonpregnant females. A better socioeconomic status did not predict better dietary intakes of iron and folate-rich foods (13). In general, the literature concerning smoking and low birth weight indicates a negative association between these factors and that food intake is decreased by smoking behavior. However, Hollingsworth et al. did not find this relationship among teenagers classified as light smokers (14). One could postulate that food intake was depressed in heavy smokers prior to pregnancy and that food consumption was not increased significantly during gestation. If the average intake is 1700-1900 kcal/day and the recommended allowances for pregnancy range from 2400 to 2700 kcal/day, then many girls must add 700-1000 kcal/day to their normal consumption patterns to meet pregnancy requirements. This study compares the dietary habits and smoking behavior of pregnant adolescents and relates these to infant birth weight and Apgar score.
Methods Sample Selection Sixty-seven pregnant volunteers were recruited from secondary schools in a northern urban city with a primarily white population (95%). Twenty-eight nonsmoking pregnant adolescents attended a special education program apart from the mainstream
JOURNAL OF ADOLESCENT HEALTH CARE Vol. 2, No. 2
population. The curriculum and services were part of the public education system. Thirty-nine pregnant smokers were enrolled from a regular public school mainstream program. Both groups received their prenatal and free and/ or reduced services at community clinics and the tertiary hospitals providing acute medical care. In addition, most participants used the free and/or reduced school lunch programs and received food stamps and other types of assistance from the community. Initial contact was made through school and clinic nurses, physicians, and brief presentations to student groups. Interested girls were then personally contacted, and the purpose of the study was explained verbally and in writing. Consent forms were signed by the teenager and the responsible adult in the family prior to entry into the study. No incentives were given for participation and no effort was made to follow up those who chose not to participate. The research protocol met the standards established by the appropriate university committee for h u m a n research. Cooperating schools, physicians, clinics, and if required, administrators of medical records provided letters of agreement.
Data Collection The initial prenatal visit for the smokers included a history and physician examination, urinalysis, hemogram, rubella titer RH and antibody levels, pap smear, and GC culture. Skinfold measurements, taken with a Lange caliper, at tricep and subscapular sites followed the National Research Council Committee on Nutritional Anthropometry procedures (15). Heights and weights were taken on a beam scale and rod and recorded in centimeters and kilograms. Skinfold measurements were not done on the nonsmoker group. For both groups, a trained nutritionist conducted the initial dietary interview, employing a standard format for asking about and recording food intake for the previous 24 hours and probing for usual food intake. Estimates of amounts eaten were compared with standardized food models. In evaluating group data, 24-hour recalls with 50 or more responses were considered adequate (16). Alcohol, tobacco, and food consumption patterns away from home were assessed by history. For the smoker group, dietary interviews and anthropometric measurements were repeated in the
December 1981
SMOKING AND PREGNANCY OUTCOME
117
Table 1. Comparison of Pregnant Adolescents: Nonsmokers vs. Smokers Onset of menses (yr)
Time between menses and conception (yr)
Location
Height (cm)
Pregravld weight (kg)
Nonsmokers (N = 28)
158.1 +_ 5.8
52.7 _+ 5.9*
12.5 + 1.1
4.0 _+ 1.6
Smokers (N = 39)
163.5 _+ 5.7
56.3 +- 8.4*
12 6 + 1.4
4.3 _+ 1 5
*P -< 0.05, mean _+ S.D.
last trimester. The sequencing of appointments and laboratory analyses throughout gestation followed protocols set up by the clinic physicians. Iron and folacin supplements were given at the initial visit, irrespective of hematologic: values. A history of chronic disease and/or previously identified obstetric problems precluded participation in the study. Infant birthweights and Apgar scores were recorded at the time of delivery and weight data were collected over a period of one to three months. Medical records and physician's files provided the most detailed information. Gestational age is not reported, since it was frequently not given in weeks and inconsistently noted in records assessible to the researchers.
Data Analyses Chi square analysis and t-test were applied to determine statistical significance for group data. Measures of central tendency were computed for nutrient and anthropometric data. Dietary data were analyzed for calories, protein, calcium, iron, ascorbic acid, vitamin A, thiamin, riboflavin, and niacin. Agriculture Handbook No. 456 provided the nutrient data base for a computerized
analysis of food records (17). Manufacturers' product information, food labels, and published estimates for nutrient density by individual researchers provided information not in the handbook (18).
Results Table 1 describes the mean values for pregravid weight and height, age at onset of menses, and the time between menses and conception. With the exception of pregravid weight, there was no statistically significant difference between the two groups. The mean chronologic age for both groups was 16.3, with a range of 13-18 years. Range for age of onset of menses was 9-16 years. Onset of menarche for both groups occurred at a mean age close to the 12.3 years published by McGanity et al (19). Both groups met the criteria for gynecologic maturity, with 4.0 years or more between menarche and conception, hence a reproductive capacity similar to that of chronologically older w o m e n (9). For purposes of this research, gynecologic age rather than chronologic age was considered the primary variable. As shown in Table 2, nonsmokers consumed more calories than light smokers but less than heavy smokers (-> 15 cigarettes/day). Protein intake ex-
T a b l e 2. M e a n Calorie I n t a k e a n d N u t r i e n t A d e q u a c y for S m o k e r s vs. N o n s m o k e r s
Item~ Calories Protein (g) Calcium (mg) Iron (mg) Vitamin A (IU) Thiamin (mg) Riboflavin (mg) Niacin (mg) Vitamin C (mg) Folic acid (/~g)
Nonsmokers (N = 28) 2146.9 89.4 1125.6 13.3 7588.5 1.3 2.1 16.1 44.8 168.0
% RDAs
Less than 15 cigarettes/day (N = 21)
88.9 114.9 93.8 74.0 151.8 96.4 130.0 100.4 158.1 21.0
1944.6 85.5 1356.1 10.1 5705.4 1.2 23 13.2 139.6 302.7
~Food and Nutrition Board: Recommended Dmtary Allowances, 8 ed., 1974.
% RDAs
More than 15 cigarettes/day (N = 18)
% RDAs
81.0 115.6 113.0 56.1 114.1 85.0 137.4 82 8 232.6 37.8
2419.8 104.5 1903.1 12.5 8050.0 1.5 3.3 17.5 173.2 249.3
99.1 126.5 158.6 69~6 161 0 106.9 195.1 107.6 288.6 36.2
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ceeded 100% of the RDAs for pregnancy and, interestingly, the heavy smokers had the highest calcium consumption. Dietary iron was two-thirds or less of the reco m m e n d e d amount for nonpregnant adolescents and much less than the 30-60 mg of elemental iron frequently prescribed. Since it is estimated that the average American diet contains about 6 mg of iron per 1000 kcal, smokers and nonsmokers had similar calorie/iron ratios based on total daily caloric intake. Dietary folacin was less than 40% of the recommended allowance for pregnancy. Although food composition tables for folacin may be subject to criticism as a reference source, the girls did not choose foods that are considered rich sources of folacin. Choices of snacking foods tended to be high in protein and low in iron and folacin. All groups exceeded allowances for vitamins A, C, and riboflavin, whereas those smoking less than 15 cigarettes per day had lower intakes of thiamin and niacin than the nonsmokers and heavy smokers. A major source of high-quality protein, calcium, and riboflavin came from free milk served at breakfast, lunch, and as an after school snack. In general, participants limited consumption of cereal products and potatoes based on a belief that those particular foods were "fattening." From 25 to 50% of calories came from foods consumed away from home and at times other than the more conventional three meals per day food pattern. Table 3 depicts the mean birth weight and maternal weight gain for smokers and nonsmokers. The N = 23 represents the girls w h o reportedly maintained their smoking behavior during pregnancy and therefore should have an infant of lower birth weight. The infants of smokers were smaller, but both groups had normal weight infants. There was no significant difference between mean birth weights of infants born to light smokers (< 15 cigarettes) and those born to heavy smokers. In terms of parity, 79.5% were first births; 15.4%, second; and 5.1%, third. Apgar scores were within normal ranges for both groups.
One case of acetonuria (1 + ) occurred in a 16-yearold subject w h o had a history of drug abuse. Her infant weighed 2580 g, the lowest birth weight recorded. Naeye reported that fetuses of mothers 10-16 years of age grew more slowly, and acetonuria was considered a marker for high perinatal mortality in undernourished gestations (20). At the initial interview, tricep and subscapular fatfolds measured 17.6 and 14.2~mm, respectively. These values are almost identical to the fatfold measurements of 51 pregnant adolescents published by Morse et al. (21). The calculated mean arm fat area fell between the 50th and 85th percentile of values published for subjects measured in the Ten State Nutrition Survey for a comparable age distribution and race. These results indicate that at the initial interview, the smoker group had mean energy stores comparable with those reported for nonpregnant adolescents.
Discussion Our results do not support the concept that smoking influences food intake, thus adversely affecting infant birth weight. The discrepancy between our results and those reported in the literature may be related to a number of factors. First, our subjects' weight gain exceeded the current standards of 25-30 lbs (22). Second, in terms of gynecologic maturity, our group was more than 4 years post menarche at conception and could be expected to perform as more mature women. Third, the social and medical support services available to both groups increased the probability that problems could be identified earlier in the smokers' group. Fourth, because of the mean birth weights of babies born to our subjects, it is unlikely that the gestational ages were shortened compared with those of older women. Perhaps smoking merely identifies the girl who is socially advanced and reacts at an early age to perceived sociental norms as compared with her
T a b l e 3. P r e g n a n c y O u t c o m e for S m o k e r s vs. N o n s m o k e r s Mean Apgar scores
Group
Infant mean birth weight (g)
Mean maternal weight gain (kg)
1 min
5 rain
Nonsmokers
3280 + 482
14.1 +- 4.8
7.0
8.5
3225 + 336
14.8 + 4.0
8.8
9.0
(N = 28) Smokers (N = 23)
December 1981
peers (23). Yerushalmy observed that w o m e n w h o become smokers t e n d e d to have low-birth-weight infants before a n d after they begin to smoke. It was suggested that the greater incidence of low-birthweight infants m a y have been due to the patient a n d not to the smoking (24). Finally, the self-selection process in a voluntary s t u d y likely reflects some intrinsic motivation and personality characteristics that m a y contribute to our positive findings of better maternal a n d fetal health. Also, the exclusion of subjects with identified obstetric problems ensures a better outcome for group comparisons a n d m a y in some w a y exclude those w h o were more malnourished. The results of the s t u d y raise a major problem about attempting to relate p r e g n a n c y outcome to a single factor, since such factors as nutrition, prenatal care, a n d maternal weight gain are all interrelated. For example, the reported calorie intake of nonpregnant adolescents in tile United States ranges from about 1750 to 1950 cal/day. For the nonsmokers and light smokers, calorie estimates were 2100 and 1900 kcal/day, respectively, m u c h lower t h a n the 2400-2700 kcal/day r e c o m m e n d e d by various professional groups (9). However, other measures such as maternal weight gain and infant birthweight were within or exceeded r e c o m m e n d e d ranges. This creates a discrepancy that is not totally explained by the vagaries of dietary data or inaccuracies associated with recording medica]Ylaboratory data. H y t t e n suggests that potential adaptation systems within the maternal melieu m a y overcome a certain a m o u n t of the nutritional a n d environmental factors (25). However, this postulation does not hold true w h e n there are d o c u m e n t e d social a n d economic factors, such as food deprivation and inadequate prenatal care, that can result in infant and maternal morbidity. Our results clearly suggest that adolescents m a y have p r e g n a n c y outcomes similar to those of chronologically older w o m e n w h e n educational, health, and nutritional support systems are available to offset the potential influence of the subject's smoking during pregnancy. Our results also demonstrate h o w important snacking patterns of adolescents can be in attaining adequate nutrition. The reported energy intake was below the r e c o m m e n d e d allowances with snacking. Thus, omitting snacks would have resulted in major deficiencies for both smokers a n d nonsmokers. Consequently, the a u t h o r believes that dietary counselors should emphasize the positive aspects of snacking to pregnant adolescents and assist t h e m in making better food choices~
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Conclusion In a s t u d y of 67 p r e g n a n t adolescents, smoking was not significantly correlated with maternal weight gain, infant birth weight, or dietary inadequacy. Pregravid weight was significantly related to low infant birth weight at the P --- 0.05 level. Smoking status was not predictive of infant birth weight or Apgar scores. Both smokers a n d n o n s m o k e r s had major dietary deficiencies of iron and folacin and t e n d e d to c o n s u m e 25-50% of their food a w a y from h o m e or in small meals rather t h a n as part of a conventional eating pattern. An adequate diet, prenatal care, a n d maternal weight gain appeared to overcome the risk of smoking for this group. The data also suggest that girls are unlikely to meet dietary allowances for iron a n d folacin t h r o u g h food consumption and that snacking is an important source of calories a n d some nutrients. Acknowledgments Grateful acknowledgment is made to Shelley Kirk, Research Assistant, and Janet Machelett, student assistant, in gathering data.
Refet'ences 1. American Cancer Society:Summary of findings from a study about cigarette smoking among teenage girls and young women. Yankelovich, Skelly and White, Inc., 1976 2. Rush D: Examination of the relationship between birth weight, cigarette smoking during pregnancy and maternal weight gain. J Obstet Gynaecol Br Commonw 81:746-752, 1974 3. Abel EL: Smoking during pregnancy: A review of effects on growth and development of offspring. Hum Bio152:593-625, 1980 4. Davies DP, Gray OP, Ellwood PC et al: Cigarette smoking in pregnancy: Associations with maternal weight gain and fetal growth. Lancet 1 (7956): 385-387, 1976 5. Garn SM, Shaw HA, McCabe KD: Relativeeffects of smoking and other variables on size of newborn. Lancet 2 (8039): 667, 1977 6. Manning FA, Feyerabend C: Cigarette smoking and fetal breathing movements. Br J Obstet Gynaeco183:262-270, 1976 7. Asmussen h Ultrastructure of the villi and fetal capillaries in placentas from smoking and non-smoking mothers. Br J Obstet Gynaecol 87:239-245, 1980 8. Food and Nutrition Board: Recommended Dietary Allowances, 9th rev. ed., 1980. National Academy of Science, 1980 9. Task Force on Adolescent Pregnancy of The American College of Obstetricians and Gynecologists.Adolescent Perinatal Health, 1979 10. Vital and Health Statistics. Dietary Intake Findings, United States, 1971-1974. Series 11, No. 202. U.S. Govt. Prtg. Office, Washington, D.C., 1977. (Pub. No. (HRA) 77-1647) 11. Food Consumption Profilesof White and BlackPersons Aged 1-74 Years. United States, 1971-74. U.S. Govt. Prtg. Office, Washington, D.C., 1979. (DHEWPub. No. (PHS) 79-1658)
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12. Ten State Nutrition Survey, 1968-1970: Parts III and IV. (DHEW Pub. No. (HSM) 72-8131, 1972) 13. Daniel WA, Gaines EG, Bennett DL: Dietary retakes and plasma concentrations of folate in healthy adolescents. Am J Clin Nutr 28:363-370, 1975 14. Hollingsworth DR, Moser RJ, Carlson JW, et al: Abnormal adolescent primiparous pregnancy: Association of race, human chorionic somatomammotropin production, and smoking. Am J Obstet Gynecol 126:230-237, 1976 15. National Research Council Committee on Nutritional Anthropometry: Body measurement and human nutrition. Detroit, Wayne University Press, 1956 16. Chalmers FW, Clayton MM, Gates LO, et al: The dietary record--How many and which days? J Am Diet Assoc 28:711-717, 1952 17. United States Department of Agriculture--Agricultural Research Service: Nutritive Value of American Foods in Common Units, Agriculture Handbook No. 456, Washington, D.C., 1975 18. Perloff BP, Butrum RR: Folacin in selected foods. J Am Diet Assoc 70:161-172, 1977
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19. McGanity WJ, Little HM, Fogelman A, et ah Pregnancy in the adolescent. I. Preliminary summary of health status. Am J Obst Gynecol 103:773-788, 1969 20. Naeye RL: Teenaged and pre-teenaged pregnancies: Consequences of the fetal-maternal competition for nutrients. Pediatrics 67:146-150, 1981 21. Morse EH, Clarke RP, Merrow SG, et al: Comparison of nutritional status of pregnant adolescents with adult pregnant women. II. Anthropometric and dietary findings. Am J Clin Nutr 28:1422-1428, 1975 22. Worthington BS: Nutrition during pregnancy, lactation and oral contraception. Nurs Clin North Am 14:269-283, 1979 23. McKinney JP, Fitzgerald HE, Strommen EA: Developmental Psychology. The Adolescent and the Young Adult. Homewood, Illinois, The Dorsey Press, 1977 24. Yerushalmy J: Infants with low birthweight born before their mothers started to smoke cigarettes. Am J Obstet Gynecol 112:277-284, 1972 25. Hytten FE: Nutrition in pregnancy. Postgrad Med J 55:295-302, 1979