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Smoking and Passive Smoking as Conditioners of Folate Status in Young Women

Departamento de Nutrición (R.M.O., A.M.R., A.M.L-S., B.N., M.C.M., B.B.), Sección
Departamental de Química Analítica (P.A.), Facultad de Farmacia, Universidad Complutense, Madrid, SPAIN

Address reprint requests to: Profa. Dra. Rosa M. Ortega, Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense, 28040-Madrid, SPAIN. E-mail: rortega{at}farm.ucm.es

	ABSTRACT

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
Objective: For women of fertile age, an adequate supply of folate is important for preventing a range of health problems, especially congenital malformations in their offspring. Since congenital deformities are more common in children of mothers who smoke, the objective was to analyse the folate status of smokers, passive smokers and non-smokers.

Methods: Folate intake was monitored in 319 women aged 18–35 (112 smokers, 100 passive smokers and 107 non-smokers) using a three day food record. Serum and erythrocyte folate concentrations were measured by radioimmunoassay. Exposure to tobacco smoke was established by a questionnaire on present and past tobacco consumption, the number of hours in contact with smokers, and by assessing urine cotinine concentrations.

Results: The folate intake of smokers (S) (159.1 ± 65.7 µg/day) and passive smokers (PS) (165.2 ± 66.6 µg/day) was lower than that of non-smokers (N) (181.7 ± 72.4 µg/day) (p < 0.05 between S and N). No subject fully met the recommended intake of the vitamin, but S and PS subjects both took less than N subjects (39.8 ± 16.4% and 41.3 ± 16.6% compared to 45.4 ± 18.1% respectively). Serum folate concentrations were also lower in S and PS subjects grouped together (16.6 ± 5.9 nmol/L) compared to N subjects (18.4 ± 6.7 nmol/L) (p < 0.05).

Conclusions: None of the studied women took the 400 µg/day of folate recommended. 6.7% had serum folate concentrations of <9.2 nmol/L. The situation was worse in S and PS subjects, which might contribute to an increased risk of developing certain diseases and to giving birth to children with congenital deformations.

Key words: smoking, women, folates, intake, serum, erythrocyte

	INTRODUCTION

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
In September 1992, the U.S. Public Health Service (PHS) recommended that women of childbearing age (i.e., those aged 15–44) who were capable of becoming pregnant ought to consume 400 µg of folic acid to reduce the number of cases of neural tube defects (NTD). Uniform compliance is estimated to decrease the incidence of NTD by up to 70% [1].

Women who smoke take fewer servings of fruits and vegetables than non-smokers, and in general their diets are more imbalanced and contain less folic acid [2–4]. This raises the question as to whether their poorer folate status has anything to do with the increased number of congenital malformations seen in their offspring [5]. Lower folate concentrations can also lead to hyper-homocysteinaemia, a known risk factor for premature birth and other complications of pregnancy [5].

According to Tribble et al. [6], passive smokers who spend several hours per day with smokers also suffer changes in their food habits and nutritional status, and develop health problems similar to those seen in smokers.

Given the importance of a good folate status in young women [7], the aim of this work was to analyze folate status in young, female smokers, passive smokers and non-smokers.

	MATERIALS AND METHODS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
The study subjects were a group of 319 women aged 18–35 (112 smokers, 100 passive smokers and 107 non-smokers). The offer to participate in the study was extended to university students and the employees of three randomly selected companies. All were informed about the characteristics of the study and all eventual subjects gave signed consent to participate. This study received the approval of the Human Research Review Committee of the Universidad Complutense of Madrid, Faculty of Pharmacy. To minimize potential bias due to special dietary intakes, the following exclusion criteria were upheld: pregnancy, lactation, vegetarianism, and the suffering of any pathology or the taking of any medication that might modify food intake.

Using the questions proposed by Pamuk et al. [8] with respect to tobacco consumption and contact with smokers, the subjects were assigned to one of three groups: non-smokers (N)—those who declared they did not smoke and had no contact with smokers, smokers (S)—those who declared they smoked, and passive smokers (PS)—those who declared themselves to be in habitual contact with smokers although not smokers themselves. Those who declared themselves sporadic smokers, to be in sporadic contact with smokers, or who had some doubt as to which group they belonged, were excluded. The number of cigarettes smoked per day was recorded, as was the number of hours of exposure to other people’s smoke (for both S and PS subjects).

The answers given in the questionnaire on smoking habits/exposure were validated by evaluating urinary continine (a sensitive biomarker of smoke exposure [9]) in 30% of subjects.

Other data were collected on all subjects as follows:

Anthropometric Survey
Weight and height (without shoes) were determined using a digital electronic weighing scale (range: 0.1–150 kg) and a digital stadiometer (range 70–205 cm). These data allowed the calculation of each subject’s body mass index (BMI, kg/m²). Waist and hip measurements were also recorded. Anthropometric dimensions were taken by trained observers following norms set by the World Health Organization (WHO) [10].

Dietary Survey
A prospective method using a "weighed food record" was followed for 3 consecutive days including a Sunday. When the record was completed, booklets were returned in person. A qualified nutritionist inspected them all to ensure they had been completed and that sufficient detail had been recorded.

The energy and nutrient contents of all food ingested were determined using the Spanish Food Composition Tables [11]. The folate intakes obtained were then compared to those recommended for young women [12].

Individual energy expenditure was estimated from the basal metabolic rate (BMR) using equations proposed by the WHO [13] and multiplying by an activity ratio [13]. Participants answered an open-ended and pretested questionnaire on their physical activity, indicating the length of time they spent sleeping, eating, studying, playing sports etc. each day [14]. The questionnaire used was applied and validated in previous studies [15]. These data were used to calculate energy expenditure [13].

An estimate of the discrepancy in reporting was obtained by subtracting estimated total energy expenditure from the self-reported energy intake. When this method is used, a negative value indicates a reported energy intake greater than the predicted total energy expenditure (possible over-reporting) and a positive value denotes a reported energy intake less than the predicted total energy expenditure (underreporting) [15,16]. The percentage of discrepancy was established using the following formula: (energy expenditure – energy intake) x 100/energy expenditure [15,16].

Hematological and Biochemical Survey
Blood tests were performed after the three days record on 235 subjects (90 smokers, 68 passive smokers and 77 non-smokers), all of whom volunteered to give samples.

Blood was drawn without stasis by venipuncture (antecubital fossa) after an overnight (12 h) fast. This was performed at the Department of Nutrition (Univ. Complutense) for the university students, and at the companies for the employees.

Whole blood was used immediately to determine red blood cell count, hematocrit index, hemoglobin concentration and mean corpuscular volume (MCV) using a Model S Coulter Counter (Coulter Electronic Limited, Luton, England) [17].

Serum (CV = 4.5%) and erythrocyte (CV = 4.9%) folate concentrations were determined using the Vitamin B-12/Folate Dual Radioassay Kit DPC (Diagnostic Product Corporation, Los Angeles, CA). A Gamma Counter 1612 (Nuclear Enterprises Ltd., Edinburgh, UK) was used to quantify results [18].

Since folate deficiency is associated with raised serum homocysteine concentrations [7,19], the latter were determined by HPLC [20]. Separation was performed in an RP-18 column (Symta, Madrid, Spain), using an intelligent pump (Merck-Hitachi L-6200 A, Hitachi, Tokyo, Japan). Detection was performed with a fluorescence spectrophotometer (Merck-Hitachi L-6200 A, Tokyo, Japan). All reagents used were supplied by Merck (Darmstad, Germany). The results were collected using a Varian 4290 (Varian, Texas USA). The inter-assay CV for homocysteine from pooled serum samples was 6.5%.

Commonly accepted hematological and biochemical standards for normal adults were used as acceptable ranges [7,21,22].

Urine samples (from early in the morning) were refrigerated and cotinine concentrations determined by ¹²⁵I radioimmunoassay in a Gamma Wallac 1470 Wizard counter (Perkin Elmer, Boston MA, USA) using the Nicotine Metabolite Kit (EUROP/DPC, Gwynedd, UK) (C.V. = 5.8%) [23].

Socioeconomic Survey
Information was collected on the subjects’ educational level, income and the characteristics of their homes [24].

Health Survey
This collected information on:

The suffering of illness (diabetes, allergies, renal or liver disease, etc.).

The consumption of medicines and/or supplements. Subjects were asked about the medicines and supplements they took (contraceptives, antacids, tranquillizers etc., as well as the quantities taken), and were asked to bring all their vitamin supplements and medications for inspection. The brand names, doses, and frequency with which the subjects used supplements were recorded.

Statistical Analyses
Means and SD are shown. Numerical differences were calculated using the Student t/ANOVA tests (where the distribution of results was homogeneous) and the Mann-Whitney/Kruskal Wallis tests (where the distribution of results was not homogeneous). The relationship between quantified parameters and cigarettes consumed/hours of exposure to smoke was investigated using linear regression. The Chi-squared test was used to establish differences between qualitative variables. Analysis of covariance was used to adjust means for age and weight and to adjust serum folic acid values according to fruit, vegetable and alcohol intake. Differences were considered significant if p < 0.05 [25].

	RESULTS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
No differences were seen among the groups with respect to personal and anthropometric data, except for age, which was a little lower in PS subjects, and weight, which was a little higher in smokers compared to N subjects (Table 1).

Folate intake in S and PS subjects was lower than in N subjects (p < 0.05 between S and N) (Table 2). This difference was maintained when adjustment was made for weight and age (analysis of covariance). Taking S and PS subjects together, folate intake (162.0 ± 66.0 µg/day) was significantly lower than in N subjects. No subject from any group took 400 µg/day—the recommended intake (RI) for women of fertile age [12]. Neither was any subject taking a supplement of this vitamin at the time of the study.

As the number of hours exposure to smoke rose, vegetable consumption fell (r = –0.2456), as did that of fruit (r = –0.2135), folate intake (r = –0.3145 with folate as µg/day and r = –0.2623 when expressed as µg/kg), and erythrocyte folate (r = –0.2267) (p < 0.05 in all cases).

Among S subjects, those who were also exposed to other people’s smoke had even lower vegetable and folate intakes, serum and erythrocyte folate concentrations, and higher homocysteine concentrations than those who were not (Table 4).

	DISCUSSION

An inherent limitation of the current study is that dietary intake was assessed by individual recall, and in this type of monitoring there is a tendency to under-report intakes [15,16]. Some authors [3] indicate that there is no published evidence regarding whether food intakes are differentially under-reported according to a person’s smoking status. The present work showed there to be a slightly greater discrepancy between energy expenditure and energy intake in S subjects, though this was not significant (Table 2). However, rather than being associated with smoking, this might be due to these subjects’ greater weight and probable greater concern over their weight [15,27]. It is reported that some women smoke as part of their strategy to lose weight [3,27].

The observed energy intake, the discrepancy in reporting and the anthropometric data obtained are similar to those seen in other groups of similar age [15,28,29]. However, folate intake (Table 2) was somewhat lower than that seen in other studies [7,28]. The present results show smoking status to be inversely associated with folate intake in women, in agreement with McPhillips et al. [2].

Many studies report a lower micronutrient intake in smokers and passive smokers compared to non-smokers/non-passive smokers [6,30,31]. However, the micronutrients most commonly studied have been antioxidants and little work has been done on the folate status in women of fertile age. Though tobacco consumption modifies food habits in the wrong direction [30,32], passive smoking can also do the same: those who live with smokers can also acquire their food habits. The obtained results (Table 4) agree with those of Trobs et al. [33] who studied 817 adults aged 27–66 allocated to one of four groups: non-smokers living with a non-smoker (Group 1), non-smokers living with a smoker (Group 2), smokers living with a non-smoker (Group 3), and smokers living with a smoker (Group 4). These authors found that plasma concentrations of homocysteine and folate (amongst other parameters) showed an unfavorable gradient from Group 1 towards Group 4. Similarly, another study on non-smoking men showed that those whose partner smoked had intakes of fruit, boiled vegetables, raw vegetables and juice that were 9%, 4%, 11%, and 17% lower, respectively, than the intakes of those whose partner was not a smoker [32].

The present serum folate results were somewhat lower than those obtained by Than et al. [34] (20.2 nmol/L) and than those recorded in women of fertile age by the 1999–2000 National Health and Nutrition Examination Survey (NHANES) (29.5 nmol/L) [35]. In agreement with Than et al. [34] the present values were lower in subjects who smoked/passively smoked (who also showed the greatest deficits) (Table 3).

The difference in serum folic acid of S + P with respect to NS is lost if adjusted by intake of fruit and vegetables, which leads to the assumption that the higher intake of fruit (not significant) and vegetables (p < 0.05) seen in NS subjects (and stated in other studies too [2–4,30,32]) can help explain the folate results observed (Table 2). Nevertheless other differences in the absorption, utilization and requirements of folate in smokers can play an important role which should be discussed further.

Serum homocysteine values (Table 3) were similar to those reported by Mennen et al. [36] (8.74 ± 2.71 µmol/L). These authors found that, in women, homocysteine was inversely related to erythrocyte folate (p = 0.11). In the present study, significant, inverse correlations were found between homocysteine and folate expressed as µg/day (r = –0.2739), folate expressed as µg/kg (r = –0.2672), serum folate (r = –0.2967) and erythrocyte folate (r = –0.2198).

O’Callaghan et al. [37] indicate that the current smokers tended to have lower levels of folate and greater homocysteine concentrations than those who had never smoked. This agrees with the present results (Table 3). In addition, the latter authors [37] showed that cigarette smokers with a plasma homocysteine above 12 µmol/L had a 12-fold increased risk of cardiovascular disease compared to non-smokers with normal plasma homocysteine concentrations. This indicates the importance of monitoring homocysteine concentrations, especially in smokers.

With respect to the number of cigarettes consumed, it has been reported that smokers of several age-race-gender categories have lower intakes of folate than non-smokers, and that intake tends to decrease as cigarette consumption increases [38]. The present study shows that those who smoked <10 cigarettes/day (14.3%) had higher serum folate concentrations (19.3 ± 5.9 nmol/L) than those who smoked more (16.0 ± 5.2 nmol/L) (p < 0.05). In addition, those who smoked <10 cigarettes/day had lower (homocysteine concentrations (8.4 ± 2.2 µmol/L) than those who smoked more (9.8 ± 2.9 µmol/L) (p < 0.05).

Cigarette smoking and exposure to tobacco smoke are associated with an increased risk of suffering a range of diseases [33,37,39]. One of the main causes behind this could be that smokers’ diets are less adequate [33,34], particularly with respect to folate intake (Table 2–Table 4).

Folate deficiency has long been thought to play a role in the etiology of cervical cancer, the third most frequent cancer among women worldwide [40]. Since it is also associated with increased homocysteine concentrations, it has also been associated with coronary heart disease risk [40].

Low plasma folate concentrations in women have been associated with an increased risk of early spontaneous abortion, preterm delivery, low birth weight, foetal growth retardation [19] and NTDs in their offspring [40,41]. A metabolic effect of folate deficiency is the elevation of blood homocysteine, and this has been associated with increased habitual spontaneous abortion and pregnancy complications such as placental abruption and preeclampsia, which increase the risk of poor pregnancy outcome [19].

Although cessation of smoking is the ideal objective, it is not always attainable. Therefore, dietary intervention with respect to folate (modifying the intake of foods or using supplements) might be a useful strategy to prevent or delay smoking-related pathologies [37,39].

	CONCLUSIONS

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
The folate status of the studied subjects was clearly inadequate: none took the recommended 400 µg/day. The status of S and PS subjects was worse, which might increase their chances of suffering a range of diseases [8] or of having babies with congenital defects [40,41].

The efficacy of folic acid in preventing of NTDs depends on it being taken before and after conception. Optimizing the compliance of women at this critical time is a public health challenge [42], and educational campaigns are needed to improve the nutritional status of this population group. The results of this study show there is a special need to get this message to smokers [2].

	FOOTNOTES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 
Supported by grants from the Ministerio de Trabajo y Asuntos Sociales, Instituto de la Mujer, Expediente 19/98.

Received August 6, 2003. Accepted March 15, 2004.

	REFERENCES

TOP FOOTNOTES ABSTRACT INTRODUCTION MATERIALS AND METHODS RESULTS CONCLUSIONS REFERENCES

 

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