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Journal of the American College of Nutrition, Vol. 17, No. 4, 379-384 (1998)
Published by the American College of Nutrition

The Influence of Smoking on Vitamin C Status During the Third Trimester of Pregnancy and on Vitamin C Levels in Maternal Milk

Rosa M. Ortega, PhD, FACN, Ana M. López-Sobaler, PhD, M. Elena Quintas, PhD, Rosa M. Martínez, PhD and Pedro Andrés, PhD

Departamento de Nutrición (R.M.O., A.M.L-S., E.Q.), Facultad de Farmacia, Universidad Complutense, Madrid SPAIN
Servicio de Análisis Clínicos, Servicio de Obstetricia y Ginecología (R.M.M.), Hospital INSALUD, Cuenca SPAIN
Laboratorio de Técnicas Instrumentales (P.A.), Facultad de Farmacia. Universidad Complutense, Madrid SPAIN

Address reprint requests to: Rosa M. Ortega, PhD, FACN, Departamento de Nutrición, Facultad de Farmacia, Universidad Complutense, 28040-Madrid SPAIN


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Objective: The aim of the present investigation was to determine the differences in vitamin C status of 57 Spanish women smokers (S) and nonsmokers (N) in their third trimester of pregnancy, and the concentrations of vitamin C in their milk.

Methods: Vitamin C intake during the third trimester was determined by recording the consumption of foods over a 5-day period (including a Sunday) and by registering vitamin C provided by dietary supplements. Vitamin C levels in maternal serum during this stage of pregnancy and in transition (days 13 to 14 of lactation) and mature milk (day 40 of lactation) were determined colorimetrically. Subjects also answered a questionnaire on their smoking habits during pregnancy.

Results: S subjects (n=16) showed a lower intake of fruits, vegetables and vitamin C than did N subjects (n=41), though these differences were not significant (17.1% of N subjects and 31.2% of S subjects took less than 80 mg of vitamin C per day). Neither were any differences found between the two groups in serum vitamin C levels. However, N subjects showed significantly greater vitamin C levels in both transition and mature milk (431.6±296.5 µmol/L and 496.1±325.6 µmol/L, respectively for N subjects, and 233.7±202.9 µmol/L and 241.3±293.1 µmol/L for S subjects). Further investigations are necessary to determine the clinical consequences of these observations, though it is already known that maternal smoking favors peroxidation events in newborn infants.

Conclusions: If the concentration of antioxidants (vitamin C) in smokers’ breast milk is also lower, this might aggravate the peroxidation problems of their newborn.

Key words: vitamin C, smoking, pregnancy, lactation, breast milk


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Several studies have indicated that the nutritional status of smokers may be compromised by an inadequate diet, and that smoking is associated with a lower intake of antioxidants, in particular vitamin C [1,2]. It has also been reported that vitamin C may be at suboptimal concentrations in the tissues and plasma of smokers [2,3]. Wald and Hackshaw [4] indicate that many of the problems observed in pregnant smokers could be due to tobacco-associated modification of their diet.

In particular, vitamin C deficiency during pregnancy has been associated with an increased risk of contracting infections, premature rupture of the membranes [5,6], prematurity [5] and eclampsia [7].

Cigarette smoking is a source of oxidant stress in pregnant women, suggesting that it could be a source of the same in infants exposed in utero [2]. At birth, the newborn is brought into an environment which is hyperoxic compared to in utero conditions and vitamin C deficiency may lead to inadequate antioxidant defenses [8]. The concentrations of antioxidants in breast milk probably defines the degree of protection it can offer against peroxidation.

The aim of the present investigation was to determine the differences in vitamin C status of Spanish women smokers and non-smokers in their third trimester of pregnancy and the concentrations of vitamin C in their milk.


   MATERIALS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The pregnancies and lactation periods of 57 women were followed. The characteristics of the subjects and criteria of inclusion/exclusion have been reported in previous papers [9–12].

The study protocol was approved by the Comité de Investigación de la Facultad de Farmacia, Universidad Complutense de Madrid and by the Comité Etico del Hospital del INSALUD de Cuenca.

During their third trimester (between weeks 32 to 36) dietary, anthropometric and biochemical studies were made. The study continued after the subjects gave birth. The composition of subjects’ (now lactating mothers) milk was analyzed at days 13 to 14 (transitional milk) and 40 (mature milk) [13].

Dietetic Survey
Food intake was recorded by keeping a ‘food record’ questionnaire for 5 days, including a Sunday. The details of the dietetic study methodology have been described in previous papers [9–12].

The vitamin C content of consumed foods was calculated using "Tables of Food Composition" published by the Instituto de Nutrición [14]. The intake of supplements was recorded by asking subjects what, and how much, they had taken during their pregnancy. This was then added to the quantity of vitamin C provided by the diet. The adequacy of vitamin C intake was determined by comparison with the recommendations for women in the second half of pregnancy as established in the "Tables of Recommended Energy and Nutrient Intakes for the Spanish Population" (80 mg/day) [15].

Estimates of 24-hour energy expenditure were made using equations proposed by the World Health Organization (WHO) [16] multiplied by an activity ratio in accordance with the criteria of several expert groups [15,16].

The percentage of discrepancy in dietary reporting was established using the following formula: (energy expenditure-energy intake)x100/energy expenditure. When this method is used, a negative value indicates a reported energy intake greater than the predicted total energy expenditure (over-reporting) and a positive value denotes a reported energy intake less than the predicted total energy expenditure (under-reporting) [17].

Biochemical Study
Blood samples were taken first thing in the morning from subjects fasted overnight. Since vitamin C is unstable in storage [18], the serum component was separated and vitamin C levels determined colorimetrically [19] (Boehringer Mannheim GMbH, Mannheim, Germany) immediately after extraction. Two samples were prepared from the collected serum. In one sample the oxidation of all reducing compounds, including L-ascorbic acid, was performed in the presence of methylsulphate-5-methylbenzene, reducing the tetrazolium salt MTT [3-(4,5-dimethylthiazoyl-2)-2,5 diphenylterazolium bromide] to give dehydroascorbic acid plus MTT-formazan. In the presence of oxygen, ascorbic acid oxidase was added to the blank sample to form dehydroascorbic acid exclusively. The color due to ascorbic acid was therefore eliminated. The difference between absorbance of the test sample and that of the blank was taken to be the quantity of ascorbic acid in the sample. The quantity of MTT-formazan was used as the measurement parameter, and was determined by the absorption recorded at 578 nm (C.V.=4.8%).

Milk samples were taken between 10 and 11 a.m. by manual expression of a 5 ml sample from each breast at the beginning and end of feeds. The protocol for both collection and subsequent handling of milk has been previously described [12]. After acidification of milk samples with citric acid to a pH of 3.5 to 4, followed by filtering [20], milk ascorbic acid levels were determined by the same method (C.V.=4.9%).

In order to establish normal limits for serum vitamin C, the criteria of the following authors were taken into account: Kübler [21] who consider values between 11.4 µmol/L y 142 µmol/L to be acceptable, Bates et al [22], who consider 17 µmol/L as the lower normal limit, and Dostálová [23], who regards <22.7 µmol/L as an indicator of high risk of deficiency, 22.7–34.1 µmol/L as a moderate risk, >34.1 µmol/L as a low risk, and >45.4 µmol/L as a very low risk (optimal situation).

With respect to vitamin C levels in maternal milk, Byerley and Kirksey [24] establish 250 µmol/L as the lower normal limit.

Anthropometric Study
Data were collected in the morning. Weight and height were determined for subjects without shoes and wearing only underwear, using a digital electronic weighing scale (Seca alpha; Rue Lavoisier 91430, Igmy, France; range: 0.1–150 Kg) and a digital stadiometer (Harpenden Pfifter 450; Badem, Padum Aveny, Carlstadt, NJ, USA; range 70–205 cm) respectively. Body mass index (BMI) (kg/m2) was calculated from these data. All data were collected by trained personnel following norms set out by the World Health Organization (WHO) [25].

In order to see how anthropometric values changed over their pregnancy, the values of these parameters at the beginning of pregnancy were taken from subjects’ clinical records. Weight and length of the newborn were measured immediately after birth.

Other Data
Gestational age at delivery was calculated from the agreed delivery data recorded by the attending obstetrician, using last menstrual period and early ultrasound examination data. Data such as age and number of children previously born were recorded in a questionnaire during the first interview.

Tobacco Consumption
Subjects were asked about their use of tobacco before they became pregnant and about any changes they had introduced when they knew they were carrying a child.

Statistical Analysis
Mean values and SD are shown. Where the distribution of results was normally distributed, the degree of significance of differences between means was calculated using the Student’s t test. Where the distribution of results was not normally distributed, the Mann-Whitney test was applied. Analysis of covariance was used to eliminate the influence of variables that could modify the results. The relationship between the number of cigarettes smoked and the concentration of vitamin C in breast milk was established by calculating the corresponding coefficients for linear correlation. Differences were considered significant if p<0.05 [26].


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
For the purpose of the present study, subjects were grouped into nonsmokers (71.9%, n=41) (N) and smokers (28.1%, n=16) (S). Table 1 shows some of the mothers’ and newborns’ personal and anthropometric data. Full details have been published in a previous paper [11]. S subjects showed lower body weights and had previously born more children, though no other significant differences were seen between the two groups.


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  		Table 1. Personal and Anthropometric Data of Subjects and Their Babies: Differences between Smokers and Nonsmokers1

 
The percentage of discrepancy in reporting was positive (10.6±19.5%) and no significant differences were observed between N (9.8±18.8%) and S subjects (12.7±21.7%).

S subjects showed a slightly lower intake of fruits (304.8±140.5 g/day) and vegetables (232.1±98.5 g/day) than did N subjects (363.7±249.2 g/day of fruits and 255.0±113.2 g/day of vegetables), though these differences were not significant. These results justify the lack of finding any significant difference between the vitamin C intakes of N and S subjects (Table 2).


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  		Table 2. Vitamin C Intake during the Third Trimester of Pregnancy

 
During the third trimester, only three S subject took a vitamin C containing supplement, in quantities of 60 to 300 mg/day. The dietetic results are, therefore, hardly modified when supplements are taken into account (Table 2).

Neither were any differences found between the two groups in serum vitamin C levels. However, N subjects showed significantly greater vitamin C levels in both transition and mature milk (Table 3).


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  		Table 3. Levels of Vitamin C in Maternal Serum during the Third Trimester and in Transition (Days 13 to 14) and Mature Milk (Day 40)

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The percentage of subjects who smoked during pregnancy (28.1%) was lower than that observed by Picone et al [27] (53.3%), similar to that recorded by Borrud et al [28], who indicate that almost a third of the pregnant women they studied were smokers, and greater than that found by Land and Stockbauer [29], who showed that during pregnancy, smoking fell from 37% of subjects in 1978 to less than 22% in 1990.

The duration of pregnancy and the anthropometric data of the mothers and their newborns (Table 1) are similar to those reported in other studies [30–32].

The intake of ascorbic acid observed during the third trimester was similar to that reported by other authors (105 mg/day [27], 102 mg/day [28], 174±81 mg/day [31], 172.5±83.2 mg/day in pregnant women with serum cholesterol <7.55 mmol/L and 181.4±81.5 mg/day in pregnant women with serum cholesterol >=7.55 mmol/L [32], 109.4 mg/day [33]).

With respect to the consumption of supplements, West et al [34] indicate that maternal use of a vitamin supplement supplying vitamin E and ascorbic acid during pregnancy may offer protection of the fetus against lead toxicity and/or free radical damage. Despite this, in the present study, the use of supplements was rare, and was observed only in three S subjects.

Though average values for ascorbic acid intake were higher than those recommended and no significant differences were seen between the two groups, 17.1% of N and 31.2% of S subjects showed ascorbic acid intakes lower than 80 mg/day.

Several studies have shown lower vitamin C intakes among smokers [1,2,31]. This was not seen in the present study, and it may be that these subjects took greater care of their diet since they were pregnant (pregnant women usually increase their consumption of fruit and vegetables [31]). Alternatively it could be due to the low consumption of cigarettes (Table 1). Only three women smoked >10/day, and only one smoked >15/day.

The concentrations of ascorbic acid in serum (Table 3) were similar to those found by Woll and Parkin [35] in Botswanan women (84.60±73.81 µmol/L, x±SD), and less than those found by the same authors among British women (269.70±109.58 µmol/L). The figures of the present study are also slightly higher than those found by Bates et al [22] (14.2–40.9 µmol/L), Dostálová [23] (34.6±15.3 µmol/L), West et al [34] (37.5–61.9 µmol/L) and Knight et al [36] (51.1±22.7 µmol/L in nulliparous African American women between 16 and 35 years of age).

The influence of ascorbic acid intake on serum levels of the vitamin has been reported by several authors [12,22,34]. In the present study, and in parallel with intake data, no differences were found in serum levels of vitamin C between N and S subjects (Table 3).

The high percentage of subjects with deficiency levels of the vitamin in serum coincides with that reported by Pfeffer et al [6], who found low levels of leucocyte vitamin C in 60 to 80% of a different group of pregnant women, independent of their weight gain and despite adequate vitamin C intake. According to Pfeffer et al [6], this may indicate a high prevalence of subclinical infections, which could be the cause of an increased vitamin C uptake by the peripheral tissues. This finding supports the notion of including biochemical estimates to detect women with "low" vitamin C levels.

The mean concentration of ascorbic acid in maternal milk (Table 3) is similar to that reported in other studies for transition milk (249.8–897.1 µmol/L [24], 300.9–346.4 µmol/L [37]) and for mature milk (369.1–408.8 µmol/L [37], 113.6–340.7 µmol/L [38], 227.1±56.8 µmol/L [39], 295.3 µmol/L [40] and 244.2–494 µmol/L [41]).

S subjects showed lower transition and mature milk vitamin C levels (Table 3). Further, a significant, negative correlation was found between the number of cigarettes smoked and the vitamin C concentration of transition (r=-0.2448) and mature milk (r=-0.1995). It would therefore seem that smoking has a more adverse effect on milk levels than serum levels of the vitamin.

Analysis of covariance shows that the differences in vitamin C concentrations in transition and mature milk between the two groups are independent of differences in pre-pregnancy body weight, or the number of children previously borne.

Bates et al [22] studied the relationship between breast milk ascorbic acid levels and intake of the same in European women, and concluded that intakes of 80 to 100 mg/day are needed to achieve levels of 284–340.7 µmol/L. However, the intake necessary to maintain satisfactory milk vitamin levels may be much higher in smokers.

The results of this study show that, though there were no differences in vitamin C intake between N and S subjects, the percentage of intakes lower than recommended was greater among S subjects (31.2% compared to 17.1% in N subjects). Some 43.9% of N subjects and 56.3% S subjects showed serum ascorbate levels of <22.7 µmol/L. Transition and mature milk levels of vitamin C were significantly higher in N subjects (Table 3).

It is clear that smoking not only influences maternal nutritional status, but as milk composition is affected, it indirectly conditions that of the descendant.

According to Hornig and Strolz [42], optimal health is a consequence of an optimum diet, and attainment of this level of health, rather than the mere prevention of deficiency symptoms, should be the goal. There can be little doubt that optimum vitamin C intakes must be greater than those which will only prevent scurvy. Further, the recommendation of different intakes might be advisable. The lowest level would be a value which would prevent deficiency symptoms. The second would be valid for healthy populations (<200 mg/day) and would take into account different needs according to age, sex, physical activity, physiological status (e.g., pregnancy or lactation), whether the patient was a smoker, pollution levels and alcohol intake. The results of the present investigation certainly suggest that recommended intakes of vitamin C for pregnant smokers should be revised.

In agreement with Borrud et al [28], it is probable that efforts to improve the nutritional status of pregnant and lactating women would be well served if all women of child bearing age were encouraged to maximize the nutritional quality of their diets. Pregnant smokers require special attention, and an increase in their consumption of fruit and vegetables is recommended. Bearing in mind the criterion of West et al [34], there may be a need to prescribe supplements of some nutrients (e.g., vitamin C) for pregnant smokers.


   ACKNOWLEDGMENTS
 
This work was supported by grants of the Fondo de Investigaciones Sanitarias de la Seguridad Social (FISss) (Spain) (Ref. 92/1181).

Received December 1, 1997. Accepted March 1, 1998.


   REFERENCES
TOP
 ABSTRACT
 INTRODUCTION
 MATERIALS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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