PEDIATRICS Vol. 107 No. 3 March 2001, pp. 540-542

Environmental Tobacco Smoke and Serum Vitamin C Levels in Children

Richard S. Strauss, MD

From the Department of Pediatrics, UMDNJ-Robert Wood Johnson School of Medicine, New Brunswick, New Jersey.

	ABSTRACT

Top Abstract Methods Results Discussion Conclusion References

Background.    High levels of free radicals in tobacco smoke are thought to be responsible for decreased levels of serum ascorbic acid in smokers and adults exposed to environmental tobacco smoke (ETS). The association of ETS to serum ascorbic acid in children is unknown.

Methods.  Data were analyzed from the Third National Health and Nutrition Examination Survey, a nationally representative sample of children and adolescents (n = 2968). Comprehensive data including serum cotinine levels and family smoking patterns allowed for analysis of relationship of ETS to serum ascorbic acid levels. Data from 24-hour dietary recall also allowed for the control of vitamin C intake. Children were divided into categories of low and high ETS exposure based on levels of serum cotinine above or below 2 ng/mL. Smokers were defined by either self-report or serum cotinine >15 ng/mL.

Results.  Although there was a trend for lower levels of vitamin C intake in children with higher levels of ETS exposure, this trend did not reach statistical significance. Among all children, serum ascorbic acid levels were linearly related to serum cotinine levels (r = 0.19). In addition, a dose-response relationship was observed between levels of tobacco exposure and serum ascorbic acid levels. After adjusting for age, gender, vitamin C intake, and multivitamin use, environmental tobacco exposure remained significantly associated with lower levels of serum ascorbic acid in children who were exposed to both high and low levels of ETS.

Conclusion.  Exposure of children to ETS leads to significant alterations in serum ascorbic acid levels. Therefore, this study further highlights the potential dangers of ETS to children.  Key words:  environmental tobacco smoke (ETS), children, adolescents, vitamin C, ascorbic acid.

In 1994, approximately 15 million children were exposed to second hand smoke.¹ Data from the first phase of the Third National Health and Nutrition Examination Survey (NHANES III) confirm that 43% of children live in a home with at least 1 smoker.² In children, there is strong evidence that exposure to environmental tobacco smoke (ETS) is associated with increased risk of respiratory illnesses,³ asthma,⁴ anesthesia complications,⁵ sudden infant death syndrome,⁶ low birth weight⁷, and adverse lipid profiles.⁸ As a result, position statements warning of the serious effects of ETS have been issued by both the American Academy of Pediatrics⁹ and the American Heart Association.¹⁰

In addition, ETS is associated with lower levels of serum vitamin C (ascorbic acid) in adults.¹¹ In a small study of 28 children exposed to ETS, serum ascorbic acid levels were also significantly lower in ETS-exposed children compared with control children.¹² Decreased serum ascorbic acid in those exposed to ETS is most likely related to the extremely high levels of free radicals in tobacco smoke that leads to depletion of biological stores of antioxidants.^11,13 For instance, Kallner and colleagues¹⁴ have demonstrated over a 40% increase in ascorbic acid turnover from free radical induced depletion in smokers compared with nonsmokers.

To address the association of ETS to serum ascorbic acid in children, data were analyzed from the Third National Health and Nutrition Examination Survey (NHANES III), a nationally representative sample of children and adults. Comprehensive data including serum cotinine levels and family smoking patterns allowed for analysis of relationship of ETS to serum ascorbic acid levels. Data from 24-hour dietary recall also allowed for the control of vitamin C intake.

	METHODS

Top Abstract Methods Results Discussion Conclusion References

Sample

The first phase of the NHANES III examined a nationally representative sample of children and adults between 1988 and 1991.^a The sample included 2968 children ages 4 through 18 with serum cotinine levels.

Smoking and Nutritional Assessment

Parents and adolescents were asked about frequency of smoking and number of cigarettes smoked per day. The total number of cigarettes smoked by household members each day were then calculated. Nutritional intake was assessed using a 24-hour diet recall for all children. Parents provided information on nutritional intake for children 11 years or younger, while children >12 years old provided their own intake. Intake of vitamin C was calculated using the US Department of Agriculture's Survey Nutrient Data Base based on the 24-hour dietary record. Interviews were conducted privately, by trained study staff, and staff performance was monitored routinely.

Laboratory Testing

Serum cotinine levels were measured using an isotope dilution, liquid chromatography, tandem mass spectrometry method. Children were categorized according to level of ETS as follows:

1. Nonexposed: No one in the household reported smoking.
2. Low exposure (ETS-Low): At least 1 parent reports smoking and serum cotinine levels <2 ng/mL.
3. High exposure (ETS-High): At least 1 parent reports smoking in the household and serum cotinine levels between 2 ng/mL and 15 ng/mL.
4. Smokers: Either self-reported smoking by child/adolescent or serum cotinine level >15 ng/mL.

Previous studies using the NHANES III data have demonstrated a 96% concordance between self-reported smoking status and serum cotinine levels above or below 15 ng/mL.¹⁵ Serum levels of ascorbic acid were measured by isocratic high-performance liquid chromatography (Waters HPLC System, Waters Chromatography Division, Milford, MA).

Statistics

The NHANES III study oversampled blacks, Hispanics, and younger adolescents. By using sample weights provided by NHANES III, the data were adjusted to account for unequal selection. Differences in proportions were assessed using ². Odds ratios (ORs) were calculated using logistic regression. Multivariate logistic regression analysis was used to assess the independent effects of smoking on nutritional intake after adjusting for age and gender. To adjust for complex sample design and clustering effects in the NHANES III sample, statistical significance was assessed using the balanced repeated replication method using the software package WesVarPC (Westat Inc, Rockville, MD).

	RESULTS

Top Abstract Methods Results Discussion Conclusion References

In the NHANES III survey, 35.3% of nonsmoking children were exposed to household smoking. An additional 11.6% of children were classified as smokers. Among children 12 years and older, 22.1% were smokers of which 55.9% were boys. Among children classified as smokers, 98.4% were 12 years or older.

Serum cotinine levels were >2 ng/mL in 2.6% of children whose parents reported no household exposure to cigarettes compared with 34.0% for nonsmoking children whose parents reported smoking (OR: 13.07; 95% confidence interval [CI]: 9.04-18.67). Of children who reported at least occasional smoking, serum cotinine levels were >2 ng/mL in 93.8% (OR: 94.63; 95% CI: 51.95-172.39). As expected, parental levels of smoking were significantly higher in children with high ETS exposure compared with children with low ETS exposure (number of cigarettes smoked by members of household/d: 25.9 ± 1.5 vs 14.2 ± 0.6; P < .001). Among children who did not report smoking, serum cotinine levels were linearly related to number of cigarettes smoked by family members (r = 0.19; P < .05). Among children who reported smoking, serum cotinine levels were also linearly related to number of cigarettes that they reported smoking per day (r = 0.42; P < .0001).

Although there was a trend for low levels of vitamin C intake in children with higher levels of ETS exposure or smoking, this trend did not reach statistical significance (vitamin C intake per day (mg)-nonexposed: 111.3 ± 3.3, ETS-low: 109.6 ± 5.4, ETS-high: 104.8 ± 5.0, smokers: 95.8 ± 7.2, F = 0.16). In addition, after adjusting for age and gender there was no difference between vitamin C intake per day between those children with no exposure to ETS and those with either low exposure (P = .82) or high exposure (P = .31). However, after adjusting for age and gender, vitamin C intake was lower among children who smoked compared with nonsmokers (P < .001). In addition, fruit intake was similar among nonsmoking children with and without ETS exposure (servings/day: 0.96 ± 0.03 vs 0.86 ± 0.06; P = .11). However, fruit intake was lower among children who smoked compared with those who did not (servings/day 0.52 ± 0.04 vs 0.92 ± 0.03; P < .001).

Among all children, serum ascorbic acid levels were linearly related to serum cotinine levels (r = 0.19; P < .001). In addition, a dose-response relationship was observed between levels of tobacco exposure and serum ascorbic acid levels (Fig 1). After adjusting for age, gender, vitamin C intake, and multivitamin use, environmental tobacco exposure remained significantly associated with lower levels of serum ascorbic acid in children who were exposed to both high and low levels of ETS (Fig 2).

View larger version (30K): [in this window] [in a new window]   Fig. 1.   Serum ascorbic acid levels in children with A, no exposure to ETS; B, low exposure (ETS-LE): at least 1 smoker in house and serum cotinine <2 ng/mL; C, high exposure (ETS-HE): at least 1 smoker in house and serum cotinine >2 ng/mL; D, smoking: either self-reported smoking by child/adolescent or serum cotinine level >15 ng/mL. Mean ± standard error of the mean.

View larger version (23K): [in this window] [in a new window]   Fig. 2.   Serum ascorbic acid levels in ETS exposed children and smoking children compared with nonsmoking, nonexposed children after controlling for age, gender, vitamin C intake, and multivitamin use. Mean ± standard error of the mean.

	DISCUSSION

Top Abstract Methods Results Discussion Conclusion References

This study demonstrates significantly lower levels of serum ascorbic acid levels in children exposed to ETS. Furthermore, a dose-response relationship was observed between ETS exposure and serum ascorbic acid with the lower levels of serum ascorbic acid in children with high levels of exposure compared with children with higher levels of exposure. Overall, serum ascorbic acid levels were approximately 20% lower in children exposed to ETS compared with those who are not exposed. Tribble and colleagues have demonstrated that adults exposed to ETS show similar results.¹¹ In addition, Jendrycczko and colleagues¹² demonstrated 50% lower ascorbic acid levels in children exposed to ETS compared with nonexposed children; however, only 28 exposed children were studied.

Decreased serum ascorbic acid in children exposed to ETS may be a result of increased rates of ascorbic acid metabolism associated with environmental tobacco exposure.¹² Decreased serum levels may also be attributable to altered dietary preferences in children and families exposed to ETS. Schiffman and colleagues¹⁶ have documented that ETS exposure attenuates both taste and smell leading to a preference for fatty foods. Similarly, Emmons and colleagues¹⁷ have demonstrated decreased vitamin C intake as well as decreased fruit and vegetable intake in adults exposed to ETS in the workplace. In this study, children who smoked reported lower levels of fruit intake; nevertheless, serum ascorbic acid remained lower among children who smoked even after adjusting for total vitamin C intake. In addition, the findings of lower levels of serum vitamin C in ETS exposed children could not be accounted for by lower levels of dietary intake because reported levels of vitamin C intake and fruit consumption were not significantly different among nonsmoking children with and without ETS exposure.

	CONCLUSION

Top Abstract Methods Results Discussion Conclusion References

Exposure of children to ETS leads to significant alterations in serum ascorbic acid levels in addition to the previously described respiratory ailments associated with ETS. This report is the first large study to document direct metabolic consequences of ETS in children. This study is, therefore, in direct contrast to continued assertions by the tobacco industry that ETS causes no damage.^18,19 Because ascorbic acid protects against plasma lipid and low-density lipoprotein oxidation,²⁰ and also appears to be important in protecting DNA from oxidative damage,²¹ this report further highlights the potential dangers of ETS to children.

	FOOTNOTES

^a Serum cotinine levels were not measured in the second phase of NHANES III (1992-1994).

Received for publication Apr 5, 2000; accepted Jun 29, 2000.

Reprint requests to (R.S.S.) Department of Pediatrics, UMDMJ-Robert Wood Johnson Medical School, One Robert Wood Johnson Pl, CN-19, New Brunswick, NJ 08903-0019. E-mail: strausrs{at}umdnj.edu

	ABBREVIATIONS

NHANES III, Third National Health and Nutrition Examination Survey; ETS, environmental tobacco smoke; OR, odds ratio; CI, 95% confidence interval.

	REFERENCES

Top Abstract Methods Results Discussion Conclusion References

1. The great American smokeout. MMWR Morb Mortal Wkly Rep. 1997;46:1037-1051
2. Pirkle JL, Flegal KM, Bernert JT, Brody DJ, Etzel RA, Mauer KR Exposure of the US population to environmental tobacco smoke. NHANES III, 1988-1991. JAMA. 1996; 275:1233-1240 [Abstract/Free Full Text]
3. Li JSM, Peat JK, Xuan W, Berry G Meta-analysis on the association between environmental tobacco smoke (ETS) exposure and the prevalence of lower respiratory tract infection in early childhood. Pediatr Pulmonol 1999; 27:5-13 [CrossRef][Medline]
4. Strachan DP, Cook DG Health effects of passive smoking. VI. Parental smoking and childhood asthma: longitudinal and case control studies. Thorax 1998; 53:204-212 [Abstract/Free Full Text]
5. Skolnick ET, Vomvolakis MA, Buck KA, Mannino SF, Sun LS Exposure to environmental tobacco smoke and the risk of adverse respiratory events in children receiving general anesthesia. Anesthesiology 1998; 88:1144-1153 [CrossRef][Medline]
6. Anderson HR, Cook DG Passive smoking and sudden infant death syndrome: review of the epidemiological evidence. Thorax 1997; 52:1003-1009 [Abstract]
7. Mainous AG, Hueston WJ. Passive smoke and low birth weight: evidence for a threshold effect. Arch Fam Med. 1994;875-878
8. Moskowitz WB, Schwartz PF, Schieken RM Childhood passive smoking, race, and coronary artery disease risk. Arch Pediatr Adolesc Med 1999; 153:446-453 [Abstract/Free Full Text]
9. American Academy of Pediatrics, Committee on Environmental Health Environmental tobacco smoke: a hazard to children. Pediatrics 1997; 99:639-642 [Abstract/Free Full Text]
10. Committee on Atherosclerosis and Hypertension in Children, American Heart Association Active and passive tobacco exposure: a serious pediatric health problem. Circulation. 1994; 90:2581-2590 [Abstract/Free Full Text]
11. Tribble DL, Giuliano LG, Formann SP Reduced plasma ascorbic acid concentrations in nonsmokers regularly exposed to environmental tobacco smoke. Am J Clin Nutr 1993; 58:886-890 [Abstract/Free Full Text]
12. Jendrycazko A, Szpyrka G, Gruszczynski J, Kozowicz M Cigarette smoke exposure of children: effect of passive smoking and vitamin E supplementation on blood antioxidant status. Neoplasma 1993; 40:199-203 [Medline]
13. Church DF, Pryor WA Free radical chemistry of cigarette smoke and its toxicological implications. Environ Health Perspect 1985; 64:111-118 [Medline]
14. Kallner AB, Harmann D, Hornig DH On the requirements of ascorbic acid in man: steady-state turnover and body pools in smokers. Am J Clin Nutr 1981; 34:1347-1355 [Abstract/Free Full Text]
15. Caraballo RS, Giovino GA, Pechacek TF, Racial and ethnic differences in serum cotinine levels of cigarette smokers: Third National Health and Nutrition Examination Survey, 1988-1991. JAMA. 1998; 280:135-139 [Abstract/Free Full Text]
16. Schiffman SS, Nagel HT Effect of environmental pollutants on taste and smell. Otolaryngol Head Neck Surg 1992; 106:693-700 [Medline]
17. Emmons KM, Thompson B, Feng Z, Hebert JR, Heimendinger J, Linnan L Dietary intake and exposure to environmental tobacco smoke in a worksite population. Eur J Clin Nutr 1995; 49:336-345 [Medline]
18. Coggins CRE, (RJ Reynolds Tobacco Company) Estimating exposure to environmental tobacco smoke. JAMA 1996; 276:603
19. Repace JL, Lowrey AH Issues and answers concerning passive smoking in the workplace: rebutting tobacco industry arguments. Tobacco Control 1992; 1:208-219
20. Frei B Ascorbic acid protects lipids in human plasma and low-density lipoprotein against oxidative damage. Am J Clin Nutr 1991; 54:1113S-1118S [Medline]
21. Fraga CG, Motchnik PA, Shigenaga MK, Helblock HJ, Jacob RA, Ames BN Ascorbic acid protect against endogenous oxidative DNA damage in human sperm. Proc Natl Acad Sci U S A 1991; 88:11003-11006 [Abstract/Free Full Text]